Ephemeral effects of El Niño–Southern Oscillation events on an eastern tropical Pacific coral community
R. Cruz-García A B , A. P. Rodríguez-Troncoso B F , F. A. Rodríguez-Zaragoza C , A. Mayfield D E and A. L. Cupul-Magaña BA Universidad Nacional Autónoma de México, Instituto de Ciencias del Mar y Limnología, Unidad Mazatlán, Capitan Joel Montes Camarena s/n, Cerro del Vigía, C.P. 82000 Mazatlan, Sinaloa, México.
B Laboratorio de Ecología Marina del Centro de Investigaciones Costeras, Centro Universitario de la Costa, Universidad de Guadalajara, Avenida Universidad 203, Puerto Vallarta, C.P. 48280, Jalisco, México.
C Laboratorio de Ecología Molecular, Microbiología y Taxonomía (LEMITAX), Departamento de Ecología, Centro Universitario de Ciencias Biológicas y Agropecuarias, Universidad de Guadalajara, Camino Ramón Padilla Sánchez, 2100 Nextipac, Zapopan, C.P. 45110, Jalisco, México.
D National Museum of Marine Biology and Aquarium, Checheng, Pingtung, Taiwan.
E Present address: Atlantic Oceanographic and Meteorological Laboratory, NOAA, Miami, FL 33149, USA.
F Corresponding author. Email: pao.rodriguezt@gmail.com
Marine and Freshwater Research 71(10) 1259-1268 https://doi.org/10.1071/MF18481
Submitted: 13 December 2018 Accepted: 4 February 2020 Published: 2 March 2020
Abstract
Coral-reef ecosystems of the central Mexican Pacific have been routinely affected by both moderate and severe El Niño–Southern Oscillation (ENSO) events over the past 20 years. Such conditions are associated with abnormally high (1997–1998, 2002–2003, 2009–2010, and 2015–2016; ‘El Niño’) and low (1999–2000, 2008–2009, and 2010–2011; ‘La Niña’) seawater temperatures. Because few studies have documented how ENSO events affect both corals and key coral competitors such as macroalgae, we evaluated the short- and long-term changes in the cover of three reef coral genera, namely, Pocillopora, Pavona and Porites, as well as four coral competitors, namely, macroalgae, turf algae, coralline algae (CCA) and sponges, over a multi-year period that encapsulated two strong ENSO events: the 2010–2011 La Niña and the 2015–2016 El Niño. Such temperature anomalies caused a short-lived decrease in coral cover, alongside a concomitant increase in CCA. The communities eventually returned to their coral-dominated states within several months of the ENSO events, suggesting that these reef habitats can recover from such episodes of anomalous seawater temperatures.
Additional keywords: benthic ecology, coralline algae, coral reefs, ENSO, Mexican Pacific, thermal stress.
References
Álvarez-Arellano, A. D., and Gaitán-Morán, J. (1994). Lagunas costeras y el litoral mexicano: geología. In ‘Lagunas Costeras y el Litoral Mexicano’. (Eds E. G. De la Lanza-Espino and C. Cáceres-Martínez.) pp. 13–74. (Universidad Autónoma de Baja California Sur: La Paz, Mexico.) [In Spanish]Anderson, M., Gorley, R. N., and Clarke, R. K. (2008). ‘PERMANOVA+ for Primer: Guide to Software and Statistical Methods.’ (Primer-E: Plymouth, UK.)
Aronson, R. B., and Precht, W. F. (2001). White-band disease and the changing face of Caribbean coral reefs. In ‘The Ecology and Etiology of Newly Emerging Marine Diseases’. (Eds P. W. Glynn, D. P. Manzello, and I. C. Enochs.) pp. 25–38. (Springer: Dordrecht, Netherlands.)
Baker, A. C., Correa, A. M., and Cunning, R. (2017). Diversity, distribution and stability of Symbiodinium in reef corals of the eastern tropical pacific. In ‘Coral Reefs of the Eastern Tropical Pacific’. (Eds P. W. Glynn, D. P. Manzello, and I. C. Enochs.) pp. 405–420. (Springer: Dordrecht, Netherlands.)
Bell, J. J., Davy, S. K., Jones, T., Taylor, M. W., and Webster, N. S. (2013). Could some coral reefs become sponge reefs as our climate changes? Global Change Biology 19, 2613–2624.
| Could some coral reefs become sponge reefs as our climate changes?Crossref | GoogleScholarGoogle Scholar | 23553821PubMed |
Bellwood, D. R., Hughes, T. P., Folke, C., and Nyström, M. (2004). Confronting the coral reef crisis. Nature 429, 827.
| Confronting the coral reef crisis.Crossref | GoogleScholarGoogle Scholar | 15215854PubMed |
Brown, B. E. (1997). Coral bleaching: causes and consequences. Coral Reefs 16, S129–S138.
| Coral bleaching: causes and consequences.Crossref | GoogleScholarGoogle Scholar |
Bruno, J. F., and Bertness, M. D. (2001). Habitat modification and facilitation in benthic marine communities. In ‘Marine Community Ecology’. (Eds M. D. Bertness, S. D. Gaines, and M. E. Hay.) pp. 201–2018. (Sinauer: Sunderland, MA, USA.)
Carriquiry, J. D., Cupul-Magaña, A. L., Rodríguez-Zaragoza, F., and Medina-Rosas, P. (2001). Coral bleaching and mortality in the Mexican Pacific during the 1997–98 El Niño and prediction from a remote sensing approach. Bulletin of Marine Science 69, 237–249.
Clarke K. R.Gorley R. N. (2006 ). ‘Primer.’ (Primer-E: Plymouth, UK.)
Comisión Nacional de Áreas Naturales Protegidas (CONANP) (2007). ‘Programa de Conservación y Manejo, Parque Nacional Islas Marietas,’ (Comisión Nacional de Áreas Naturals Protegidas: México.)
Connell, J. H. (1997). Disturbance and recovery of coral assemblages. Coral Reefs 16, S101–S113.
| Disturbance and recovery of coral assemblages.Crossref | GoogleScholarGoogle Scholar |
Corado-Nava, N. A., Rodríguez, D., and Rivas, G. (2014). Efecto de la colonización de los céspedes algales en el crecimiento de Pocillopora capitata (Anthozoa: Scleractinia) en el Pacífico tropical mexicano. Revista Mexicana de Biodiversidad 85, 1086–1092.
| Efecto de la colonización de los céspedes algales en el crecimiento de Pocillopora capitata (Anthozoa: Scleractinia) en el Pacífico tropical mexicano.Crossref | GoogleScholarGoogle Scholar |
Cortés, J., Murillo, M. M., Guzmán, H. M., and Acuña, J. (1984). Pérdida de zooxantelas y muerte de corales y otros organismos arrecifales en el Caribe y Pacífico de Costa Rica. Revista de Biología Tropical 32, 227–231.
Crowder, L. B., and Cooper, W. E. (1982). Habitat structural complexity and the interaction between bluegills and their prey. Ecology 63, 1802–1813.
| Habitat structural complexity and the interaction between bluegills and their prey.Crossref | GoogleScholarGoogle Scholar |
Cruz, I. C., Waters, L. G., Kikuchi, R. K., Leão, Z. M., and Turra, A. (2018). Marginal coral reefs show high susceptibility to phase shift. Marine Pollution Bulletin 135, 551–561.
| Marginal coral reefs show high susceptibility to phase shift.Crossref | GoogleScholarGoogle Scholar | 30301073PubMed |
Cupul-Magaña, A. (2008). Estructura ecológica y patrones de colonización en las comunidades coralinas y arrecifes de la región de Bahía de Banderas, costa sur e Islas de Nayarit. Ph.D. Dissertation, Universidad Autónoma de Nayarit, Nayarit, México.[In Spanish]
Cupul-Magaña, A. L., and Rodríguez-Troncoso, A. P. (2017). Tourist carrying capacity at Islas Marietas National Park: an essential tool to protect the coral community. Applied Geography 88, 15–23.
| Tourist carrying capacity at Islas Marietas National Park: an essential tool to protect the coral community.Crossref | GoogleScholarGoogle Scholar |
Davies, P. S. (1984). The role of zooxanthellae in the nutritional energy requirements of Pocillopora eydouxi. Coral Reefs 2, 181–186.
De La Lanza-Espino, G., and Cáceres Martínez, C. (1994). ‘Lagunas Costeras y el Litoral Mexicano.’ No. 551.4609 L3. [In Spanish]
Díaz-Pulido, G., McCook, L. J., Dove, S., Berkelmans, R., Roff, G., Kline, D. I., and Weekss, Díaz-Pulido, G., McCook, L. J., Dove, S., Berkelmans, R., Roff, G., Kline, D. I., and Weekss, Díaz-Pulido, G., McCook, L. J., Dove, S., Berkelmans, R., Roff, G., Kline, D. I., and Weekss, Díaz-Pulido, G., McCook, L. J., Dove, S., Berkelmans, R., Roff, G., Kline, D. I., and Weekss, (2009). Doom and boom on a resilient reef: climate change, algal overgrowth and coral recovery. PLoS One 4, e5239.
| Doom and boom on a resilient reef: climate change, algal overgrowth and coral recovery.Crossref | GoogleScholarGoogle Scholar | 19384423PubMed |
Gardner, T. A., Côté, I. M., Gill, J. A., Grant, A., and Watkinson, A. R. (2003). Long-term region-wide declines in Caribbean corals. Science 301, 958–960.
| Long-term region-wide declines in Caribbean corals.Crossref | GoogleScholarGoogle Scholar | 12869698PubMed |
Gates, R. D., Baghdasarian, G., and Muscatine, L. (1992). Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching. The Biological Bulletin 182, 324–332.
| Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching.Crossref | GoogleScholarGoogle Scholar | 29304594PubMed |
Glynn, P. W. (1984). Widespread coral mortality and the 1982–83 El Niño warming event. Environmental Conservation 11, 133–146.
| Widespread coral mortality and the 1982–83 El Niño warming event.Crossref | GoogleScholarGoogle Scholar |
Glynn, P. W. (1993). Coral reef bleaching: ecological perspectives. Coral Reefs 12, 1–17.
| Coral reef bleaching: ecological perspectives.Crossref | GoogleScholarGoogle Scholar |
Glynn, P. W., and Ault, J. S. (2000). A biogeographic analysis and review of the far eastern Pacific coral reef region. Coral Reefs 19, 1–23.
| A biogeographic analysis and review of the far eastern Pacific coral reef region.Crossref | GoogleScholarGoogle Scholar |
Glynn, P. W., and Colley, S. B. (2001). A collection of the studies on the effects of the 1997-98 El Niño Southern Oscillation event on corals and coral reefs in the Eastern Tropical Pacific. Bulletin of Marine Science 69, 288.
Glynn, P. W., Mones, A. B., Podestá, G. P., Colbert, A., and Colgan, M. W. (2017). El Niño–Southern Oscillation: effects on eastern Pacific coral reefs and associated biota. In ‘Coral Reefs of the Eastern Tropical Pacific’. (Eds P. W. Glynn, D. P. Manzello, and I. C. Enochs.) pp. 251–290. (Springer: Dordrecht, Netherlands.)
Harrington, L., Fabricius, K., De’Ath, G., and Negri, A. (2004). Recognition and selection of settlement substrata determine post‐settlement survival in corals. Ecology 85, 3428–3437.
| Recognition and selection of settlement substrata determine post‐settlement survival in corals.Crossref | GoogleScholarGoogle Scholar |
Hernández-Zulueta, J., Rodríguez-Zaragoza, F. A., Araya, R., Vargas-Ponce, O., Rodríguez-Troncoso, A. P., Cupul-Magaña, A. L., Díaz-Pérez, L., Ríos-Jara, E., and Ortiz, M. (2017). Multi-scale analysis of hermatypic coral assemblages at Mexican central Pacific. Scientia Marina 81, 91–102.
| Multi-scale analysis of hermatypic coral assemblages at Mexican central Pacific.Crossref | GoogleScholarGoogle Scholar |
Hughes, T. P. (1985). Life histories and population dynamics of early successional corals. In ‘Proceedings 5th International Coral Reef Symposium, Vol. 4’. French Polynesia. pp. 101–106.
Hughes, T. P., and Connell, J. H. (1999). Multiple stressors on coral reefs: a long‐term perspective. Limnology and Oceanography 44, 932–940.
| Multiple stressors on coral reefs: a long‐term perspective.Crossref | GoogleScholarGoogle Scholar |
Hughes, T. P., Baird, A. H., Bellwood, D. R., Card, M., Connolly, S. R., Folke, C., Grosberg, R., Hoegh-Guldberg, O., Jackson, J. B. C., Kleypas, J., Lough, J. M., Marshall, P., Nyström, M., Palumbi, S. R., Pandolfi, J. M., Rosen, B., and Roughgarden, J. (2003). Climate change, human impacts, and the resilience of coral reefs. Science 301, 929–933.
| Climate change, human impacts, and the resilience of coral reefs.Crossref | GoogleScholarGoogle Scholar | 12920289PubMed |
Hughes, T. P., Anderson, K. D., Connolly, S. R., Heron, S. F., Kerry, J. T., Lough, J. M., Baird, A. H., Baum, J. K., Berumen, M. L., Bridge, T. C., Clarr, D. C., Eackin, C. M., Gilmour, J. P., Graham, N. A. J., Harrison, H., Hobbs, J.-P., Hoewy, A. S., Hoogenboom, H., Lowe, H. J., McCulloch, M. T., Pandolfi, J. M., Pratchett, M., Schoepf, V., Torda, G., and Wilson, S. K. (2018). Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83.
| Spatial and temporal patterns of mass bleaching of corals in the Anthropocene.Crossref | GoogleScholarGoogle Scholar | 29302011PubMed |
Idjadi, J. A., and Edmunds, P. J. (2006). Scleractinian corals as facilitators for other invertebrates on a Caribbean reef. Marine Ecology Progress Series 319, 117–127.
| Scleractinian corals as facilitators for other invertebrates on a Caribbean reef.Crossref | GoogleScholarGoogle Scholar |
Lindquist, S. (1986). The heat-shock response. Annual Review of Biochemistry 55, 1151–1191.
| The heat-shock response.Crossref | GoogleScholarGoogle Scholar | 2427013PubMed |
López-Pérez, A., Guendulain-García, S., Granja-Fernández, R., Hernández-Urraca, V., Galván-Rowland, L., Zepeta-Vilchis, R., and López-López, D. (2016). Reef community changes associated with the 2009–2010 El Niño in the southern Mexican Pacific. Pacific Science 70, 175–190.
| Reef community changes associated with the 2009–2010 El Niño in the southern Mexican Pacific.Crossref | GoogleScholarGoogle Scholar |
Loya, Y., Sakai, K., Yamazato, K., Nakano, Y., Sambali, H., and van Woesik, R. (2001). Coral bleaching: the winners and the losers. Ecology Letters 4, 122–131.
| Coral bleaching: the winners and the losers.Crossref | GoogleScholarGoogle Scholar |
McClanahan, T. R. (2004). The relationship between bleaching and mortality of common corals. Marine Biology 144, 1239–1245.
| The relationship between bleaching and mortality of common corals.Crossref | GoogleScholarGoogle Scholar |
McClanahan, T., Polunin, N., and Done, T. (2002). Ecological states and the resilience of coral reefs. Conservation Ecology 6, 18.
| Ecological states and the resilience of coral reefs.Crossref | GoogleScholarGoogle Scholar |
McClanahan, T. R., Weil, E., Cortés, J., Baird, A. H., and Ateweberhan, M. (2009). Consequences of coral bleaching for sessile reef organisms. In ‘Coral Bleaching’. (Eds J. Madeleine, H. van Oppen, and J. Lough.) pp. 121–138. (Springer-Verlag: Berlin, Germany.)
McManus, J. W., and Polsenberg, J. F. (2004). Coral–algal phase shifts on coral reefs: ecological and environmental aspects. Progress in Oceanography 60, 263–279.
| Coral–algal phase shifts on coral reefs: ecological and environmental aspects.Crossref | GoogleScholarGoogle Scholar |
Muscatine, L., and Porter, J. W. (1977). Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27, 454–460.
| Reef corals: mutualistic symbioses adapted to nutrient-poor environments.Crossref | GoogleScholarGoogle Scholar |
Nava, H., and Carballo, J. L. (2013). Environmental factors shaping boring sponge assemblages at Mexican Pacific coral reefs. Marine Ecology 34, 269–279.
| Environmental factors shaping boring sponge assemblages at Mexican Pacific coral reefs.Crossref | GoogleScholarGoogle Scholar |
Palacios-Hernández, E., Carrillo, L. E., Filonov, A., Brito-Castillo, L., and Cabrera-Ramos, C. E. (2010). Seasonality and anomalies of sea surface temperature off the coast of Nayarit, Mexico. Ocean Dynamics 60, 81–91.
Pandolfi, J. M., Bradbury, R. H., Sala, E., Hughes, T. P., Bjorndal, K. A., Cooke, R. G., McArdle, D., McClenachan, L., Newman, M. J. H., Paredes, G., Warner, R. R., and Jackson, J. B. C. (2003). Global trajectories of the long-term decline of coral reef ecosystems. Science 301, 955–958.
| Global trajectories of the long-term decline of coral reef ecosystems.Crossref | GoogleScholarGoogle Scholar | 12920296PubMed |
Pantoja, D. A., Marinone, S. G., Parés-Sierra, A., and Gómez-Valdivia, F. (2012). Numerical modeling of seasonal and mesoscale hydrography and circulation in the Mexican central Pacific. Ciencias Marinas 38, 363–379.
| Numerical modeling of seasonal and mesoscale hydrography and circulation in the Mexican central Pacific.Crossref | GoogleScholarGoogle Scholar |
Podestá, G. P., and Glynn, P. W. (1997). Sea surface temperature variability in Panamá and Galápagos: extreme temperatures causing coral bleaching. Journal of Geophysical Research. Oceans 102, 15749–15759.
| Sea surface temperature variability in Panamá and Galápagos: extreme temperatures causing coral bleaching.Crossref | GoogleScholarGoogle Scholar |
Rasher, D. B., and Hay, M. E. (2010). Chemically rich seaweeds poison corals when not controlled by herbivores. Proceedings of the National Academy of Sciences of the United States of America 107, 9683–9688.
| Chemically rich seaweeds poison corals when not controlled by herbivores.Crossref | GoogleScholarGoogle Scholar | 20457927PubMed |
Reyes-Bonilla, H., Carriquiry, J., Leyte-Morales, G., and Cupul-Magaña, A. (2002). Effects of the El Niño–Southern Oscillation and the anti-El Niño event (1997–1999) on coral reefs of the western coast of México. Coral Reefs 21, 368–372.
| Effects of the El Niño–Southern Oscillation and the anti-El Niño event (1997–1999) on coral reefs of the western coast of México.Crossref | GoogleScholarGoogle Scholar |
Reyes-Bonilla, H., Calderón-Aguilera, L. E., Cruz-Piñón, G., López-Pérez, R. A., and Medina-Rosas, P. (2010). Evaluación de la diversidad gama de corales arrecifales (Scleractinia) en el Pacífico de México. Revista Mexicana de Biodiversidad 81, 113–121.
| Evaluación de la diversidad gama de corales arrecifales (Scleractinia) en el Pacífico de México.Crossref | GoogleScholarGoogle Scholar |
Robinson, G. (1985). The influence of the 1982–1983 El Niño on Galápagos marine life. In ‘El Niño in the Galápagos Island: the 1982–1983 Event’. (Eds G. Robinson and E. M. Del Pino.) pp. 153–190. (Charles Darwin Foundation for the Galápagos Islands: Quito, Ecuador.)
Rodríguez-Troncoso, A. P., Carpizo-Ituarte, E., Pettay, D. T., Warner, M. E., and Cupul-Magaña, A. L. (2014). The effects of an abnormal decrease in temperature on the eastern Pacific reef-building coral Pocillopora verrucosa. Marine Biology 161, 131–139.
| The effects of an abnormal decrease in temperature on the eastern Pacific reef-building coral Pocillopora verrucosa.Crossref | GoogleScholarGoogle Scholar |
Rodríguez-Troncoso, A. P., Carpizo‐Ituarte, E., and Cupul‐Magaña, A. L. (2016). Physiological response to high temperature in the tropical eastern Pacific coral Pocillopora verrucosa. Marine Ecology 37, 1168–1175.
| Physiological response to high temperature in the tropical eastern Pacific coral Pocillopora verrucosa.Crossref | GoogleScholarGoogle Scholar |
Roff, G., Chollett, I., Doropoulos, C., Golbuu, Y., Steneck, R. S., Isechal, A. L., van Woesik, R., and Mumby, P. J. (2015). Exposure-driven macroalgal phase shift following catastrophic disturbance on coral reefs. Coral Reefs 34, 715–725.
| Exposure-driven macroalgal phase shift following catastrophic disturbance on coral reefs.Crossref | GoogleScholarGoogle Scholar |
Rouzé, H., Lecellier, G., Langlade, M. J., Planes, S., and Berteaux-Lecellier, V. (2015). Fringing reefs exposed to different levels of eutrophication and sedimentation can support similar benthic communities. Marine Pollution Bulletin 92, 212–221.
| Fringing reefs exposed to different levels of eutrophication and sedimentation can support similar benthic communities.Crossref | GoogleScholarGoogle Scholar | 25586642PubMed |
Schönberg, C. H. L., and Wilkinson, C. R. (2001). Induced colonization of corals by a clionid bioeroding sponge. Coral Reefs 20, 69–76.
| Induced colonization of corals by a clionid bioeroding sponge.Crossref | GoogleScholarGoogle Scholar |
Sheppard, R. C. C., Davy, S. K., and Pilling, G. M. (2010). ‘The Biology of Coral Reefs.’ (Oxford University Press: New York, USA.)
Smith, J. E., Shaw, M., Edwards, R. A., Obura, D., Pantos, O., Sala, E., Sandin, S. A., Smriga, S., Hataya, M., and Rohwer, F. L. (2006). Indirect effects of algae on coral: algae‐mediated, microbe‐induced coral mortality. Ecology Letters 9, 835–845.
| Indirect effects of algae on coral: algae‐mediated, microbe‐induced coral mortality.Crossref | GoogleScholarGoogle Scholar | 16796574PubMed |
Sotelo-Casas, R. C., Cupul-Magaña, A. L., Rodríguez-Zaragoza, F. A., Solís-Marín, F. A., and Rodríguez-Troncoso, A. P. (2018). Structural and environmental effects on an assemblage of echinoderms associated with a coral community. Marine Biodiversity 48, 1401–1411.
| Structural and environmental effects on an assemblage of echinoderms associated with a coral community.Crossref | GoogleScholarGoogle Scholar |
Steele, M. A. (1999). Effects of shelter and predators on reef fishes. Journal of Experimental Marine Biology and Ecology 233, 65–79.
| Effects of shelter and predators on reef fishes.Crossref | GoogleScholarGoogle Scholar |
ter Braak, C. J., and Smilauer, P. (2002). CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 4.5). Available at: www.canoco.com.
Tribollet, A., and Golubic, S. (2011). Reef bioerosion: agents and processes. In ‘Coral Reefs: an Ecosystem in Transition’. pp. 435–449. (Springer: Dordrecht, Netherlands.)
Wilkinson, C. (2000). ‘Status of Coral Reefs of the World: 2000.’ Global Coral Reef Monitoring Network, Townsville, Qld, Australia.
Wyrtki, K. (1965). Surface currents of the eastern tropical Pacific Ocean. Inter-American Tropical Tuna Commission Bulletin 9, 268–305.