Nursery-reared coral outplanting success in an upwelling-influenced area in Costa Rica
DOI:
https://doi.org/10.15517/rev.biol.trop..v71iS1.54879Keywords:
Bahía Culebra; coral reef; coral gardening; Eastern Tropical Pacific; ecological restoration; growth rate.Abstract
Introduction: Environmental and intrinsic factors such as seawater temperature, salinity, nutrient concentration, upwelling, species, and life history can influence coral outplant survival and growth, and in consequence, the effectiveness of restoration. Thus, it is key to understand how these factors can shape coral outplant performance to ensure the long-term success of a restoration program.
Objective: To establish the survival and growth rate of outplanted coral nursery-reared colonies of branching Pocillopora spp. and massive corals Pavona gigantea, Pavona clavus, and Porites lobata in Bahía Culebra, North Pacific of Costa Rica, and to determine whether the site of origin of the coral fragment and the presence of seasonal upwelling affected the growth of Pocillopora outplants.
Methods: From September 2020 to September 2021, we monitored the survival, health, and growth of 30 Pocillopora spp. colonies from six donor sites, and 31 fragments of massive species (P. gigantea [n = 18], P. clavus [n = 8], P. lobata [n = 5]) that were outplanted to a degraded reef. We recorded in situ seawater temperature, salinity, and nutrient concentration.
Results: By the end of the year, 100 % of the Pocillopora spp. outplants survived. Survival was 71.4 % for P. clavus, 47.5 % for P. gigantea, and 20 % for P. lobata. Coral tissue loss and predation marks were observed at least once in 71 % of massive outplants. Pocillopora spp. colonies increased their initial area in 333.1 %, at a rate of 9.98 ± 1.69 cm yr-1. The site of origin of the outplant influenced growth rate, but not the presence of seasonal upwelling. Massive species fragments grew at a rate of 1.35 ± 0.24 cm yr-1 for P. clavus, 1.48 ± 0.21 cm yr-1 for P. gigantea, and 0.61 cm yr-1 for P. lobata, with no differences among them.
Conclusions: Environmental conditions at site level allow for high survival and growth of Pocillopora spp. outplants, previously considered as sensitive to stressors, and point towards acclimation to seasonal upwelling. Although survival of massive species was lower, developing a multi-species approach is key to enhance restoration success.
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Afiq-Rosli, L., Taira, D., Loke, H.X., Toh, T.C., Toh, K.B., Ng, C.S.L., Cabaitan, P.C., Chou, L.M., & Song, T. (2017). In situ nurseries enhance coral transplant growth in sedimented waters. Marine Biology Research, 13(8), 878–887. DOI: https://doi.org/10.1080/17451000.2017.1307988
Alvarado, J. J., Beita-Jiménez, A., Mena, S., Fernández-García, C., Cortés, J., Sánchez-Noguera, C., Jiménez, C., & Guzmán-Mora, A. G. (2018). Cuando la conservación no puede seguir el ritmo del desarrollo: Estado de salud de los ecosistemas coralinos del Pacífico Norte de Costa Rica. Revista de Biología Tropical, 66(S1), 280–308. DOI: https://doi.org/10.15517/rbt.v66i1.33300
Alvarado, J. J., Cortés, J., Guzmán, H., & Reyes-Bonilla, H. (2016). Density, size, and biomass of Diadema mexicanum (Echinoidea) in Eastern Tropical Pacific coral reefs. Aquatic Biology, 24, 151–161. DOI: https://doi.org/10.3354/ab00645
Alvarado, J. J., Cortés, J., & Reyes-Bonilla, H. (2012). Reconstruction of Diadema mexicanum bioerosion impact on three Costa Rican Pacific coral reefs. Revista de Biología Tropical, 60(S2), 121–132. DOI: https://doi.org/10.15517/rbt.v60i2.19975
Arnold, S. N., Steneck, R. S., & Mumby, P. J. (2010). Running the gauntlet: inhibitory effects of algal turfs on the processes of coral recruitment. Marine Ecology Progress Series, 414, 91–105. DOI: https://doi.org/10.3354/meps08724
Baums, I. B., Baker, A. C., Davies, S. W., Grottoli, A. G., Kenkel, C. D., Kitchen, S. A., Kuffner, I. B., LaJeunesse, T. D., Matz, M. V., Miller, M. W., Parkinson, J. E., & Shantz, A. A. (2019). Considerations for maximizing the adaptive potential of restored coral populations in the western Atlantic. Ecological Applications, 29(8), e01978. DOI: https://doi.org/10.1002/eap.1978
Bayraktarov, E., Banaszak, A. T., Montoya-Maya, P., Kleypas, J., Arias-González, J. E., Blanco, M., Calle-Triviño, J., Charuvi, N., Cortés-Useche, C., Galván, V., García-Salgado, M. A., Gnecco, M., Guendulain-García, S. D., Hernández-Delgado, E. A., Marín-Moraga, J. A., Maya, M. F., Mendoza-Quiroz, S., Mercado-Cervantes, S., Morikawa, M., Nava, G. ... Frías-Torres, S. (2020). Coral reef restoration efforts in Latin American countries and territories. PLoS ONE, 15 (8), e0228477. DOI: https://doi.org/10.1371/journal.pone.0228477
Bezy, M. B. (2009). Reproducción sexual y reclutamiento del coral masivo Pavona clavus en Bahía Culebra, Golfo de Papagayo, Costa Rica [Unpublished master’s thesis]. Universidad de Costa Rica.
Boström-Einarsson, L., Babcock, R. C., Bayraktarov, E., Ceccarelli, D., Cook, N., Ferse, S. C. A., Hancock, B., Harrison, P., Hein, M., Shaver, E., Smith, A., Suggett, D., Stewart-Sinclair, P. J., Vardi, T., & McLeod, I. M. (2020). Coral restoration – A systematic review of current methods, successes, failures and future directions. PLoS ONE, 15(1), e0226631. DOI: https://doi.org/10.1371/journal.pone.0226631
Cano, I., Sellares-Blasco, R. I., Lefcheck, J. S., Villalpando, M. F., & Croquer, A. (2021). Effects of herbivory by the urchin Diadema antillarum on early restoration success of the coral Acropora cervicornis in the central Caribbean. Journal of Experimental Marine Biology and Ecology, 539, 151541. DOI: https://doi.org/10.1016/j.jembe.2021.151541
Chomitz, B. (2021). The coral-associated fauna and sessile benthic reef community of Pocillopora coral colonies following transplantation in Golfo Dulce, South Pacific, Costa Rica: Composition, dynamics and succession [Unpublished master’s thesis]. Universidad de Costa Rica.
Coles, S. L., & Jokiel, P. L. (1978). Synergistic effects of temperature, salinity and light on the hermatypic coral Montipora verrucosa. Marine Biology, 49, 187–195. DOI: https://doi.org/10.1007/BF00391130
Combillet, L., Fabregat-Malé, S., Mena, S., Marín-Moraga, J. A., Gutiérrez, M., & Alvarado, J. J. (2022). Pocillopora spp. growth analysis on restoration structures in an Eastern Tropical Pacific upwelling area. PeerJ, 10, e13248. DOI: https://doi.org/10.7717/peerj.13248
Cortés, J., & Jiménez, C. (2003). Corals and coral reefs of the Pacific of Costa Rica: history, research and status. In J. Cortés (Ed.), Latin American Coral Reefs (pp. 361-367). Elsevier Science. DOI: https://doi.org/10.1016/B978-044451388-5/50017-5
Cortés, J., Jiménez, C. E., Fonseca, A. C, & Alvarado, J. J. (2010). Status and conservation of coral reefs in Costa Rica. Revista de Biología Tropical, 58(S1), 33–50. DOI: https://doi.org/10.15517/rbt.v58i1.20022
Cruz-García, R., Rodríguez-Troncoso, A. P., Rodríguez-Zaragoza, F. A., Mayfield, C. A. & Cupul-Magaña, A. L. (2020). Ephemeral effects of El Niño–Southern Oscillation events on an eastern tropical Pacific coral community. Marine and Freshwater Research, 71(10), 1259–1268. DOI: https://doi.org/10.1071/MF18481
Cupul-Magaña, A. L., & Calderón-Aguilera, L. (2008). Cold water bleaching at Islas Marietas National Park, Nayarit, Mexico. XV Oceanography National Meeting, Veracruz, Mexico.
D’Angelo, C., & Wiedenmann, J. (2014). Impacts of nutrient enrichment on coral reefs: new perspectives and implications for coastal management and reef survival. Current Opinion in Environmental Sustainability, 7, 82–93. DOI: https://doi.org/10.1016/j.cosust.2013.11.029
Dang, V. D. H., Cheung, P. Y., Fong, C. L., Mulla, A. J., Shiu, J. H., Lin, C. H., & Nozawa, Y. (2020) Sea urchins play an increasingly important role for coral resilience across reefs in Taiwan. Frontiers in Marine Science, 7, 581945. DOI: https://doi.org/10.3389/fmars.2020.581945
Drury, C., Manzello, D. P., & Lirman, D. (2017). Genotype and local environment dynamically influence growth, disturbance response and survivorship in the threatened coral, Acropora cervicornis. PLoS ONE, 12, e0174000. DOI: https://doi.org/10.1371/journal.pone.0174000
Edmunds, P. J., & Putnam, H. M. (2020). Science-based approach to using growth rate to assess coral performance and restoration outcomes. Biology Letters, 1, 20200227. DOI: https://doi.org/10.1098/rsbl.2020.0227
Edwards, A. J. (2010). Reef rehabilitation manual. Coral reef targeted research & capacity building for Management Program. St Lucia, Australia.
Faxneld, S., Jörgensen, T. L., & Tedengren, M. (2010). Effects of elevated seawater temperature, reduced salinity and nutrient enrichment on metabolism of the coral Turbinaria mesenterina. Estuarine, Coastal and Shelf Science, 88(4), 482–487. DOI: https://doi.org/10.1016/j.ecss.2010.05.008
Fernández, C. (2007). Propagación del alga Caulerpa sertularioides (Chlorophyta) en Bahía Culebra, Golfo de Papagayo, Pacífico norte de Costa Rica [Unpublished master’s thesis]. Universidad de Costa Rica.
Fernández-García, C., Cortés, J., Alvarado, J. J., & Nívia-Ruiz, J. (2012). Physical factors contributing to the benthic dominance of the algae Caulerpa sertularioides (Caulerpaceae, Clorophyta) in the upwelling Bahía Culebra, North Pacific of Costa Rica. Revista de Biología Tropical, 60, 93–107. DOI: https://doi.org/10.15517/rbt.v60i2.19970
Ferse, S. C. A., Hein, M. Y., & Rölfer L. (2021). A survey of current trends and suggested future directions in coral transplantation for reef restoration. PLoS ONE, 16(5), e0249966. DOI: https://doi.org/10.1371/journal.pone.0249966
Foo, S. A, & Asner, G. P. (2020). Sea surface temperature in coral reef restoration outcomes. Environmental Research Letters, 15, 074045. DOI: https://doi.org/10.1088/1748-9326/ab7dfa
Foo, S. A., & Asner, G. P. (2021). Impacts of remotely sensed environmental drivers on coral outplant survival. Restoration Ecology, 29(1), e13309. DOI: https://doi.org/10.1111/rec.13309
Forrester, G. E., Ferguson, M. A., O’Connell-Rodwell, C. E., & Jarecki, L. L. (2014). Long-term survival and colony growth of Acropora palmata fragments transplanted by volunteers for restoration. Aquatic Conservation: Marine and Freshwater Ecosystems, 24, 81–91. DOI: https://doi.org/10.1002/aqc.2374
Forrester, G. E., Maynard, A., Schofield, S., & Taylor, K. (2012). Evaluating causes of transplant stress in fragments of Acropora palmata used for coral reef restoration. Bulletin of Marine Science, 88(4), 1099–1113. DOI: https://doi.org/10.5343/bms.2012.1016
Forsman, Z. H., Page, C. A., Toonen, R. J., & Vaughan, D. (2015). Growing coral larger and faster: micro-colony-fusion as a strategy for accelerating coral cover. PeerJ, 3, e1313. DOI: https://doi.org/10.7717/peerj.1313
Gerstle, L. (2020). Growth and transgenerational acclimatization of juvenile Pocillopora damicornis [Unpublished doctoral dissertation]. University of Hawai’i. DOI: https://doi.org/10.1101/2020.11.02.364596
Glynn, P., & Ault, J. (2000). A biogeographic analysis and review of the far eastern Pacific coral reef region. Coral Reefs, 19, 1–23. DOI: https://doi.org/10.1007/s003380050220
Glynn, P. W., Colley, S. B., Carpizo-Ituarte, E., & Richmond, R. H. (2017). Coral reproduction in the Eastern Pacific. In P. W. Glynn, D. P. Manzello, I. C. Enochs (Eds.), Coral Reefs of the Eastern Tropical Pacific (Vol 8, pp. 435–476). Springer Science+Business Media. DOI: https://doi.org/10.1007/978-94-017-7499-4_15
Goergen, E. A., & Gilliam, D. S. (2018). Outplanting technique, host genotype, and site affect the initial success of outplanted Acropora cervicornis. PeerJ, 6, e4433. DOI: https://doi.org/10.7717/peerj.4433
Graham, N. A. J., Jennings, S., MacNeil, M. A., Mouillot, D., & Wilson, S. K. (2015). Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature, 518, 1–17. DOI: https://doi.org/10.1038/nature14140
Guzmán, H. (1991). Restoration of coral reefs in Pacific Costa Rica. Conservation Biology, 5(2), 189–195. DOI: https://doi.org/10.1111/j.1523-1739.1991.tb00123.x
Hein, M. Y., Willis, B. E., Beeden, R., & Birtles, A. (2017). The need for broader ecological and socioeconomic tools to evaluate the effectiveness of coral restoration programs. Restoration Ecology, 25(6), 873–883. DOI: https://doi.org/10.1111/rec.12580
Herrera-Escalante, T., López-Pérez, R. A., & Leyte-Morales, G. E. (2005). Bioerosion caused by the sea urchin Diadema mexicanum (Echinodermata: Echinoidea) at Bahías de Huatulco, Western Mexico. Revista de Biología Tropical, 53(S3), 263–273.
Hughes, T. P., Kerry, J., Álvarez-Noriega, M., Álvarez-Romero, J. G., Anderson, K. D., Baird, A. H., Babcock, R. C., Beger, M., Bellwood, D. R., Berkelmans, R., Bridge, T. C., Butler, I. R., Byrne, M., Cantin, N. E., Comeau, S., Connolly, S. R., Cumming, G. S., Dalton, S. J., Diaz-Pulido, G., … Wilson, S. K. (2017). Global warming and recurrent mass bleaching of corals. Nature, 543, 373–377. DOI: https://doi.org/10.1038/nature21707
Hughes, T. P., Kerry, J. T., Baird, A. H. Connolly, S. R., Chase, T. J., Dietzel, A., Hill, T., Hoey, A. S., Hoogenboom, M. O., Jacobson, M., Kerswell, A., Madin, J. S., Mieog, A., Paley, A. S., Pratchett, M. S., Torda, G., Woods, R. M. (2019). Global warming impairs stock–recruitment dynamics of corals. Nature, 568, 387–390. DOI: https://doi.org/10.1038/s41586-019-1081-y
Hughes, T. P., Rodrigues, M. J., Bellwood, D. R., Ceccarelli, D., Hoegh-Guldberg, O., McCook, L., Moltschaniwskyj, N., Pratchett, M. S., Steneck, R. S., & Willis, B. (2007). Phase shifts, herbivory, and the resilience of coral reefs to climate change. Current Biology, 17(4), 360–365. DOI: https://doi.org/10.1016/j.cub.2006.12.049
Ishida-Castañeda, J., Pizarro, V., López-Victoria, M., & Zapata, F. A. (2020). Coral reef restoration in the Eastern Tropical Pacific: feasibility of the coral nursery approach. Restoration Ecology, 28(1), 22–28. DOI: https://doi.org/10.1111/rec.13047
Jiménez, C. (1997). Corals and coral reefs of Culebra Bay, Pacific coast of Costa Rica: anarchy in the reef [Paper presentation]. In H.A. Lessios & I.A. Macintyre (Eds.), Proceedings of the VIII International Coral Reef Symposium [Symposium], VIII International Coral Reef Symposium, Panama.
Jiménez, C. (2001). Arrecifes y ambientes coralinos de Bahía Culebra, Pacífico de Costa Rica: aspectos biológicos, económicos, recreativos y de manejo. Revista de Biología Tropical, 49(S2), 215–231.
Jiménez, C. (2007). Arrecifes coralinos, ¿víctimas de los cambios? Ambientico, 171, 5–7.
Jiménez, C., Bassey, G., Segura, Á., & Cortés, J. (2010). Characterization of the coral communities and reefs of two previously undescribed locations in the upwelling region of Gulf of Papagayo (Costa Rica). Revista Ciencias Marinas y Costeras, 2, 95–108. DOI: https://doi.org/10.15359/revmar.2.8
Jiménez, C., & Cortés, J. (2003). Growth of seven species of scleractinian corals in an upwelling environment of the Eastern Pacific (Golfo de Papagayo, Costa Rica). Bulletin of Marine Science, 72, 187–198.
Kleypas, J. A., & Yates, K. K. (2009). Coral reefs and ocean acidification. Oceanography, 22(4), 108–117. DOI: https://doi.org/10.5670/oceanog.2009.101
Kleypas, J. A., McManus, J. W., & Meñez L. A. B. (1999). Environmental limits to coral reef development: Where do we draw the line? American Zoologist, 39(1), 146–159. DOI: https://doi.org/10.1093/icb/39.1.146
Kodera, S. M., Edwards, C. B., Petrovic, V., Pedersen, N. E., Eynaud, Y., & Sandin, S. A. (2020). Quantifying life history demographics of the scleractinian coral genus Pocillopora at Palmyra Atoll. Coral Reefs, 39, 1091–1105. DOI: https://doi.org/10.1007/s00338-020-01940-8
Koval, G., Rivas, N., D’Alessandro, M., Hesley, D., Santos, R., & Lirman, D. (2020). Fish predation hinders the success of coral restoration efforts using fragmented massive corals. PeerJ, 8, e9978. DOI: https://doi.org/10.7717/peerj.9978
Ladd, M. C., Miller, M. W., Hunt, J. H., Sharp, W. C., & Burkpile, D. E. (2019). Harnessing ecological processes to facilitate coral restoration. Frontiers in Ecology and the Environment, 16(4), 239–247. DOI: https://doi.org/10.1002/fee.1792
Liñán-Cabello, M. A., Flores-Ramírez, L. A., Laurel-Sandoval, M. A., García-Mendoza, E., Soriano-Santiago, O., & Delgadillo-Nuño, M. A. (2011). Acclimation in Pocillopora spp. during a coral restoration program in Carrizales Bay, Colima, Mexico. Marine and Freshwater Behaviour and Physiology, 44(1), 61–72. DOI: https://doi.org/10.1080/10236244.2010.537440
Lirman, D., & Schopmeyer, S. (2016). Ecological solutions to reef degradation: optimizing coral reef restoration in the Caribbean and Western Atlantic. PeerJ, 4, e2597. DOI: https://doi.org/10.7717/peerj.2597
Lirman, D., Schopmeyer, S., Galvan, V., Drury, C., Baker, A. C., & Baums, I. B. (2014). Growth dynamics of the threatened Caribbean staghorn coral Acropora cervicornis: influence of host genotype, symbiont identity, colony size, and environmental setting. PLoS ONE, 9(9), e107253. DOI: https://doi.org/10.1371/journal.pone.0107253
Lirman, D., Schopmeyer, S., Manzello, D., Gramer, L. J., Precht, W. F., Muller-Karger, F., Banks, K., Barnes, B., Bartels, E., Bourque, A., Byrne, J., Donahue, S., Duquesnel, J., Fisher, L., Gilliam, D., Hendee, J., Johnson, M., Maxwell, K., McDevitt, E., Monty, J., Rueda, D., Ruzicka, R., & Thanner, S. (2011). Severe 2010 cold-water event caused unprecedented mortality to corals of the Florida reef tract and reversed previous survivorship patterns. PLoS ONE, 6(8), e23047. DOI: https://doi.org/10.1371/journal.pone.0023047
Lirman, D., Thyberg, T., Herlan, J., Hill, C., Young-Lahiff, C., Schopmeyer, S., Huntington, B., Santos, R., & Drury, C. (2010). Propagation of the threatened staghorn coral Acropora cervicornis: methods to minimize the impacts of fragment collection and maximize production. Coral Reefs, 29, 729–735. DOI: https://doi.org/10.1007/s00338-010-0621-6
Lizcano-Sandoval, L. D., Londoño-Cruz, E., & Zapata, F. A. (2018). Growth and survival of Pocillopora damicornis (Scleractinia: Pocilloporidae) coral fragments and their potential for reef restoration in the Tropical Eastern Pacific. Marine Biology Research, 14, 887–897. DOI: https://doi.org/10.1080/17451000.2018.1528011
Lohr, K. E., Ripple, K., & Patterson, J. T. (2020). Differential disturbance effects and phenotypic plasticity among outplanted corals at patch and fore reef sites. Journal for Nature Conservation, 55, 125827. DOI: https://doi.org/10.1016/j.jnc.2020.125827
Lough, J. M., & van Oppen, M. J. H. (2018). Introduction: coral bleaching-patterns, processes, causes and consequences. In M. J. H. van Oppen, & J. M. Lough (Eds.), Coral Bleaching, Patterns, processes, causes, and consequences (pp. 1–8). Springer. DOI: https://doi.org/10.1007/978-3-319-75393-5_1
Lustic, C., Maxwell, K., Bartels, E., Reckenbeil, B., Utset, E., Schopmeyer, S., Zink, I., & Lirman, D. (2020). The impacts of competitive interactions on coral colonies after transplantation: A multispecies experiment from the Florida Keys, US. Bulletin of Marine Science, 96(4), 805–818. DOI: https://doi.org/10.5343/bms.2019.0086
Miller, M. W., Lohr, K. E., Cameron, C. M., Williams, D. E., & Peters, E. C. (2014). Disease dynamics and potential mitigation among restored and wild staghorn coral, Acropora cervicornis. PeerJ, 2, e541. DOI: https://doi.org/10.7717/peerj.541
Omori, M. (2019). Coral restoration research and technical developments: what we have learned so far. Marine Biology Research, 15(7), 377–409. DOI: https://doi.org/10.1080/17451000.2019.1662050
Page, C. A., Muller, E. M., & Vaughan, D. E. (2018). Microfragmenting for the successful restoration of slow growing massive corals. Ecological Engineering, 123, 86–94. DOI: https://doi.org/10.1016/j.ecoleng.2018.08.017
Palacios, M. M., Muñoz, C. G., & Zapata, F. A. (2014). Fish corallivory on a pocilloporid reef and experimental coral responses to predation. Coral Reefs, 33, 625–636. DOI: https://doi.org/10.1007/s00338-014-1173-y
Pinzón, J. H., & LaJeunesse, T. C. (2011). Species delimitation of common reef corals in the genus Pocillopora using nucleotide sequence phylogenies, population genetics and symbiosis ecology. Molecular Ecology, 20(2), 311–325. DOI: https://doi.org/10.1111/j.1365-294X.2010.04939.x
Pinzón, J. H., Sampayo, E., Cox, E., Chauka, L. J., Chen, C. A., Voolstra, C. R., & LaJeunesse, T. C. (2013). Blind to morphology: genetics identifies several widespread ecologically common species and few endemics among Indo-Pacific cauliflower corals (Pocillopora, Scleractinia). Journal of Biogeography, 40(8), 1595–1608. DOI: https://doi.org/10.1111/jbi.12110
Precht, W. F. (2006). Coral reef restoration handbook: the rehabilitation of an ecosystem under siege. CRC Press. DOI: https://doi.org/10.1201/9781420003796
R Core Team (2021). R: A language and environment for statistical computing [Computer software]. R Foundation for Statistical Computing. http://www.r-project.org/index.html
Rinkevich, B. (1995). Restoration strategies for coral reefs damaged by recreational activities: The use of sexual and asexual recruits. Restoration Ecology, 3(4), 241–251. DOI: https://doi.org/10.1111/j.1526-100X.1995.tb00091.x
Rinkevich, B. (2014). Rebuilding coral reefs: does active reef restoration lead to sustainable reefs? Current Opinion in Environmental Sustainability, 7, 28–36. DOI: https://doi.org/10.1016/j.cosust.2013.11.018
Rivas, N., Hesley, D., Kaufman, M., Unsworth, J., D’Alessandro, M., & Lirman, D. (2021). Developing best practices for the restoration of massive corals and the mitigation of predation impacts: influences of physical protection, colony size, and genotype on outplant mortality. Coral Reefs, 40, 1227–1241. DOI: https://doi.org/10.1007/s00338-021-02127-5
Rixen, T., Jiménez, C., & Cortés, C. (2012). Impact of upwelling events on the sea water carbonate chemistry and dissolved oxygen concentration in the Gulf of Papagayo (Culebra Bay), Costa Rica: Implications for coral reefs. Revista de Biología Tropical, 60(S2), 187–195. DOI: https://doi.org/10.15517/rbt.v60i2.20004
Rodríguez-Sáenz, K., & Rodríguez-Fonseca, J. (2004). Avistamientos del delfín manchado, Stenella attenuata (Cetacea: Delphinidae) en Bahía Culebra, Costa Rica, 1999-2000. Revista de Biología Tropical, 49(2), 189–193.
Rodríguez-Troncoso, A. P., Carpizo-Ituarte, E., & Cupul-Magaña, A. L. (2010). Differential response to cold and warm water conditions in Pocillopora colonies from the Central Mexican Pacific. Journal of Experimental Marine Biology and Ecology, 391(1–2), 57–64. DOI: https://doi.org/10.1016/j.jembe.2010.06.006
Rodríguez-Troncoso, A. P., Carpizo-Ituarte, E., & Cupul-Magaña, A. L. (2016). Physiological response to high temperature in the Tropical Eastern Pacific coral Pocillopora verrucosa. Marine Ecology, 37(5), 1168–1175. DOI: https://doi.org/10.1111/maec.12392
Rodríguez-Troncoso, A. P., Carpizo-Ituarte, E., Pettay, D. T., Warner, M. E., & 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. DOI: https://doi.org/10.1007/s00227-013-2322-5
Romero-Torres, M., Acosta, A., Palacio-Castro, A. M., Treml, E. A., Zapata, F. A., Paz-García, D. A., & Porter, J. W. (2020). Coral reef resilience to thermal stress in the Eastern Tropical Pacific. Global Change Biology, 26(7), 3880–3890. DOI: https://doi.org/10.1111/gcb.15126
Roth, F., Saalmann, F., Thomson, T., Coker, D. J., Villalobos, R., Jones, B. H., Wild, C., & Carvalho, S. (2018). Coral reef degradation affects the potential for reef recovery after disturbance. Marine Environmental Research, 142, 48–58. DOI: https://doi.org/10.1016/j.marenvres.2018.09.022
Sánchez-Noguera, C. (2012). Cambios socioeconómicos y ambientales en Bahía Culebra, Guanacaste, Costa Rica: implicaciones para su gestión [Unpublished master's tesis]. Universidad de Costa Rica.
Sánchez-Noguera, C. (2019). Carbonate chemistry and coral reefs in the Pacific coast of Costa Rica [Unpublished doctoral dissertation]. Universität Hamburg.
Sánchez-Noguera, C., Jiménez, C., & Cortés, J. (2018a). Desarrollo costero y ambientes marino-costeros en Bahía Culebra, Guanacaste, Costa Rica. Revista de Biología Tropical, 66(S1), 309–327. DOI: https://doi.org/10.15517/rbt.v66i1.33301
Sánchez-Noguera, C., Stuhldreier, I., Cortés, J., Jiménez, C., Morales, Á., Wild, C., & Rixen, T. (2018b). Natural ocean acidification at Papagayo upwelling system (north Pacific Costa Rica): implications for reef development. Biogeosciences, 15, 2349–2360. DOI: https://doi.org/10.5194/bg-15-2349-2018
Schopmeyer, S. A., & Lirman, D. (2015). Occupation dynamics and impacts of damselfish territoriality on recovering populations of the threatened staghorn coral, Acropora cervicornis. PLoS ONE, 10(11), e0141302. DOI: https://doi.org/10.1371/journal.pone.0141302
Shafir, S., & Rinkevich, B. (2013). Mariculture of coral colonies for the public aquarium sector. In R. J. Leewis, & M. Janse (Eds.), Advances in coral husbandry in public aquariums (Vol 2, pp. 315–318). Burgers’ Zoo.
Stuhldreier, I., Sánchez-Noguera, C., Roth, C., Cortés, J., Rixen, T., & Wild, C. (2015). Upwelling increases net primary production of corals and reef-wide gross primary production along the Pacific coast of Costa Rica. Frontiers in Marine Science, 2, 113. DOI: https://doi.org/10.3389/fmars.2015.00113
Tortolero-Langarica, J. J. A., Cupul-Magaña, A. L., & Rodríguez-Troncoso, A. P. (2014). Restoration of a degraded coral reef using a natural remediation process: A case study from a Central Mexican Pacific National Park. Ocean & Coastal Management, 96, 12–19. DOI: https://doi.org/10.1016/j.ocecoaman.2014.04.020
Tortolero-Langarica, J. J. A, Rodríguez-Troncoso, A. P., Cupul-Magaña, A. L., & Carricart-Ganivet, J. P. (2017). Calcification and growth rate recovery of the reef-building Pocillopora species in the northeast tropical Pacific following an ENSO disturbance. PeerJ, 5, e3191. DOI: https://doi.org/10.7717/peerj.3191
Tortolero-Langarica, J. J. A., Rodríguez-Troncoso, A. P., Cupul-Magaña, A. L., Alarcón-Ortega, L. C., Santiago-Valentín, J. D. (2019). Accelerated recovery of calcium carbonate production in coral reefs using low-tech ecological restoration. Ecological Engineering, 128, 89–97. DOI: https://doi.org/10.1016/j.ecoleng.2019.01.002
Tortolero-Langarica, J. J. A., Rodríguez-Troncoso, A. P., Cupul-Magaña, A. L., & Rinkevich, B. (2020). Micro-fragmentation as an effective and applied tool to restore remote reefs in the Eastern Tropical Pacific. International Journal of Environmental Research and Public Health, 17, 6574. DOI: https://doi.org/10.3390/ijerph17186574
Tortolero-Langarica, J. J. A., Rodríguez-Troncoso, A. P., Cupul-Magaña, A. L., Morales-de-Anda, D. E., Caselle, J. E., & Carricart-Ganivet, J. P. (2022). Coral calcification and carbonate production in the eastern tropical Pacific: The role of branching and massive corals in the reef maintenance. Geobiology, 20(4), 533–545. DOI: https://doi.org/10.1111/gbi.12491
Trygonis, V., & Sini, M. (2012). PhotoQuad: A dedicated seabed image processing software, and a comparative error analysis of four photoquadrat methods. Journal of Experimental Marine Biology and Ecology, 424–425, 99–108. DOI: https://doi.org/10.1016/j.jembe.2012.04.018
Unsworth, J. D., Hesley, D., D’Alessandro, M., & Lirman, D. (2020). Outplanting optimized: Developing a more efficient coral attachment technique using Portland cement. Restoration Ecology, 29(1), e13299. DOI: https://doi.org/10.1111/rec.13299
van Oppen, M. J. H., & Blackall, L. L. (2019). Coral microbiome dynamics, functions and design in a changing world. Nature Reviews Microbiology, 17, 557–567. DOI: https://doi.org/10.1038/s41579-019-0223-4
van Oppen, M. J. H., Oliver, J. K., Putnam, H. M., & Gates, R. D. (2015). Building coral reef resilience through assisted evolution. Proceedings of the National Academy of Sciences, 112, 2307–2313. DOI: https://doi.org/10.1073/pnas.1422301112
van Woesik, R., Ripple, K., & Miller, S. L. (2017). Macroalgae reduces survival of nursery-reared Acropora corals in the Florida reef tract. Restoration Ecology, 26(3), 563–569. DOI: https://doi.org/10.1111/rec.12590
Ware, M., Garfield, E. N., Nedimyer, K., Levy, J., Kaufman, L., Precht, W., Winters, R. S., & Miller, S. L. (2020). Survivorship and growth in staghorn coral (Acropora cervicornis) outplanting projects in the Florida Keys National Marine Sanctuary. PLos ONE, 15(5), e0231817. DOI: https://doi.org/10.1371/journal.pone.0231817
Wiedenmann, J., D’Angelo, C., Smith, E.G., Hunt, A. N., Legiret, F. E., Postle, A. D., & Achterberg, E. P. (2013). Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nature Climate Change, 3, 160–164. DOI: https://doi.org/10.1038/nclimate1661
Ziegler, M., Roder, C. M., Büchel, C., & Voolstra, C. R. (2014). Limits to physiological plasticity of the coral Pocillopora verrucosa from the central Red Sea. Coral Reefs, 33, 1115–1129. DOI: https://doi.org/10.1007/s00338-014-1192-8
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