Effects of thermal stress caused by the 2015–2016 El Niño on the biochemical composition, exoskeleton structure, and symbiont density of the fire coral Millepora alcicornis

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Norma Olguín-López
Víctor H Hernández-Elizárraga
Rosalina Hernández-Matehuala
Juana I Rojas-Molina
Ramón Guevara-Gonzalez
César Ibarra-Alvarado
Alejandra Rojas Molina


Reef-forming cnidarians are essential for maintaining ecological balance. Unfortunately, coral reefs are endangered due to coral bleaching, which interrupts mutualistic symbiosis between Symbiodiniaceae algae and their coral hosts. Bleaching events result in very high coral mortality and the rapid deterioration of reef structures. Studies aimed at explaining the causes, mechanisms, and consequences of coral bleaching have been mainly conducted with anthozoans, while the impacts of thermal stress responsible for coral bleaching have been scarcely studied in hydrozoans, such as Millepora species (phylum Cnidaria, class Hydrozoa), which are the second most important reef-forming cnidarians. In the present study, the effects of thermal stress caused by the 2015–2016 El Niño on symbiont abundance, exoskeleton structure, and the biochemical composition of Millepora alcicornis were analyzed. Unbleached M. alcicornis specimens exhibited a higher abundance of Breviolum and Durisdinium species, which suggests that unbleached hydrocoral colonies might counteract thermal stress by hosting thermotolerant symbionts of the Durisdinium genus. Bleached hydrocorals exhibited lower levels of calcification than unbleached hydrocorals as well as changes in the microstructure of trabeculae and zooid pores. In contrast, thermal stress did not affect total calcium carbonate and carbohydrate content. Bleached tissues showed significantly higher levels of protein and refractory material, whereas their lipid content decreased considerably. The present study provides evidence that bleached M. alcicornis colonies suffered a decline in calcification and changes in the structure of their exoskeletons after being exposed to the 2015–2016 El Niño. The significant decrease in lipid content suggests that M. alcicornis primarily uses energy stores to maintain vital cellular processes at the expense of calcification.


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Olguín-López, N., Hernández-Elizárraga, V. H., Hernández-Matehuala, R., Rojas-Molina, J. I., Guevara-Gonzalez, R., Ibarra-Alvarado, C., & Rojas Molina, A. (2023). Effects of thermal stress caused by the 2015–2016 El Niño on the biochemical composition, exoskeleton structure, and symbiont density of the fire coral Millepora alcicornis. Ciencias Marinas, 49. https://doi.org/10.7773/cm.y2023.3296



Aichelman HE, Townsend JE, Courtney TA, Baumann JH, Davies SW, Castillo KD. 2016. Heterotrophy mitigates the response of the temperate coral Oculina arbuscula to temperature stress. Ecol Evol. 6(18):6758-6769. https://doi.org/10.1002/ece3.2399 DOI: https://doi.org/10.1002/ece3.2399

Ainsworth TD, Heron SF, Ortiz JC, Mumby PJ, Grech A, Ogawa D, Eakin CM, Leggat W. 2016. Climate change disables coral bleaching protection on the Great Barrier Reef. Science. 352(6283):338-342. https://doi.org/10.1126/science.aac7125 DOI: https://doi.org/10.1126/science.aac7125

Anthony KRN, Helmstedt KJ, Bay LK, Fidelman P, Hussey KE, Lundgren P, Mead D, McLeod IM, Mumby PJ, Newlands M, et al. 2020. Interventions to help coral reefs under global change—A complex decision challenge. Plos one. 15:e0236399. https://doi.org/10.1371/journal.pone.0236399 DOI: https://doi.org/10.1371/journal.pone.0236399

Anthony KRN, Hoogenboom MO, Maynard JA, Grottoli AG, Middlebrook R. 2009. Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Funct Ecol. 23(3):539-550. https://doi.org/10.1111/j.1365-2435.2008.01531.x DOI: https://doi.org/10.1111/j.1365-2435.2008.01531.x

Baker AC, Correa AMS, Cunning R. 2017. Chapter 13—Diversity, distribution and stability of Symbiodinium reef corals of the Eastern Tropical Pacific, Persistance and Loss in a Dynamic Environment. In: Glynn PW, Manzello DP, Enochs IC (eds.), Coral Reefs of the Eastern Tropical Pacific, Coral Reefs of the World. Netherlands: Springer. p. 405-420. https://doi.org/10.1007/978-94-017-7499-4 DOI: https://doi.org/10.1007/978-94-017-7499-4_13

Bay RA, Palumbi SR. 2015. Rapid acclimation ability mediated by transcriptome changes in reef-building corals. GBE. 7(6):1602-1612. https://doi.org/10.1093/gbe/evv085 DOI: https://doi.org/10.1093/gbe/evv085

Colombo-Pallotta MF, Rodríguez-Román A, Iglesias-Prieto R. 2010. Calcification in bleached and unbleached Montastraea faveolata: evaluating the role of oxygen and glycerol. Coral Reefs. 29:899-907. https://doi.org/10.1007/s00338-010-0638-x DOI: https://doi.org/10.1007/s00338-010-0638-x

Connolly SR, Lopez-Yglesias MA, Anthony KRN. 2012. Food availability promotes rapid recovery from thermal stress in a scleractinian coral. Coral Reefs. 31:951-960. https://doi.org/10.1007/s00338-012-0925-9 DOI: https://doi.org/10.1007/s00338-012-0925-9

Correa AMS, McDonald MD, Baker AC. 2009. Development of clade-specific Symbiodinium primers for quantitative PCR (qPCR) and their application to detecting clade D symbionts in Caribbean corals. Mar Biol. 156:2403-2411. https://doi.org/10.1007/s00227-009-1263-5 DOI: https://doi.org/10.1007/s00227-009-1263-5

Davy SK, Allemand D, Weis VM. 2012. Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev. 76(2):229-261. https://doi.org/10.1128/MMBR.05014-11 DOI: https://doi.org/10.1128/MMBR.05014-11

De Salvo MK, Sunagawa S, Voolstra CR, Medina M. 2010. Transcriptomic responses to heat stress and bleaching in the elkhorn coral Acropora palmata. Mar Ecol Prog Ser. 402:97-113. https://doi.org/10.3354/meps08372 DOI: https://doi.org/10.3354/meps08372

Desalvo MK, Voolstra CR, Sunagawa S, Schwarz JA, Stillman JH, Coffroth MA, Szmant AM, Medina M. 2008. Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol Ecol. 17(17):3952-3971. https://doi.org/10.1111/j.1365-294X.2008.03879.x DOI: https://doi.org/10.1111/j.1365-294X.2008.03879.x

D’Olivo JP, McCulloch MT. 2017. Response of coral calcification and calcifying fluid composition to thermally induced bleaching stress. Sci Rep. 7:2207. https://doi.org/10.1038/s41598-017-02306-x DOI: https://doi.org/10.1038/s41598-017-02306-x

Eakin CM, Sweatman HPA, Brainard RE. 2019. The 2014–2017 global-scale coral bleaching event: insights and impacts. Coral Reefs. 38:539-545. https://doi.org/10.1007/s00338-019-01844-2 DOI: https://doi.org/10.1007/s00338-019-01844-2

Foster NL, Attrill MJ. 2021. Chapter 20 - Changes in coral reef ecosystems as an indication of climate and global change. In: Letcher TM (ed.), Climate Change, Observed Impacts on Planet Earth. 3rd ed. Amsterdam (The Netherlands): Elsevier. p. 427-443. https://doi.org/10.1016/B978-0-12-821575-3.00020-7 DOI: https://doi.org/10.1016/B978-0-12-821575-3.00020-7

Frank U, Brickner I, Rinkevich B, Loya Y, Bak RPM, Achituv Y, Ilan M. 1995. Allogeneic and xenogeneic interactions in reef-building corals may induce tissue growth without calcification. Mar Ecol Prog Ser. 124:181-188. https://doi.org/10.3354/meps124181 DOI: https://doi.org/10.3354/meps124181

Fransolet D, Roberty S, Plumier JC. 2012. Establishment of endosymbiosis: The case of cnidarians and Symbiodinium. J Exp Mar Biol Ecol. 420–421:1-7. https://doi.org/10.1016/j.jembe.2012.03.015 DOI: https://doi.org/10.1016/j.jembe.2012.03.015

García-Arredondo A, Rojas-Molina A, Ibarra-Alvarado C, Iglesias-Prieto, R. 2011. Effects of bleaching on the pharmacological and toxicological activities elicited by the aqueous extracts prepared from two “fire corals” collected in the Mexican Caribbean. J Exp Mar Biol Ecol. 396(2):171-176. https://doi.org/10.1016/j.jembe.2010.10.021 DOI: https://doi.org/10.1016/j.jembe.2010.10.021

Grottoli AG, Rodrigues LJ, Juarez C. 2004. Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event. Mar Biol. 145:621-631. https://doi.org/10.1007/s00227-004-1337-3 DOI: https://doi.org/10.1007/s00227-004-1337-3

Grottoli AG, Rodrigues LJ, Palardy JE. 2006. Heterotrophic plasticity and resilience in bleached corals. Nature. 440:1186-1189. https://doi.org/10.1038/nature04565 DOI: https://doi.org/10.1038/nature04565

Grottoli AG, Warner ME, Levas SJ, Aschaffenburg MD, Schoepf V, McGinley M, Baumann J, Matsui Y. 2014. The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Glob Chang Biol. 20(12):3823-3833. https://doi.org/10.1111/gcb.12658 DOI: https://doi.org/10.1111/gcb.12658

Harland AD, Davies PS, Fixter LM. 1992. Lipid content of some Caribbean corals in relation to depth and light. Mar Biol. 113:357-361. https://doi.org/10.1007/BF00349159 DOI: https://doi.org/10.1007/BF00349159

Hernández-Elizárraga VH, Olguín-López N, Hernández-Matehuala R, Ocharán-Mercado A, Cruz-Hernández A, Guevara-González RG, Caballero-Pérez J, Ibarra-Alvarado C, Sánchez-Rodríguez J, Rojas-Molina A. 2019. Comparative analysis of the soluble proteome and the cytolytic activity of unbleached and bleached Millepora complanata (“Fire Coral”) from the Mexican Caribbean. Mar drugs. 17(7):393. https://doi.org/10.3390/md17070393 DOI: https://doi.org/10.3390/md17070393

Hillyer KE, Dias D, Lutz A, Roessner U, Davy SK. 2018. 13C metabolomics reveals widespread change in carbon fate during coral bleaching. Metabolomics. 14:12. https://doi.org/10.1007/s11306-017-1306-8 DOI: https://doi.org/10.1007/s11306-017-1306-8

Hillyer KE, Dias DA, Lutz A, Wilkinson SP, Roessner U, Davy SK. 2017. Metabolite profiling of symbiont and host during thermal stress and bleaching in the coral Acropora aspera. Coral Reefs. 36:105-118. https://doi.org/10.1007/s00338-016-1508-y DOI: https://doi.org/10.1007/s00338-016-1508-y

Hillyer KE, Tumanov S, Villas-Bôas S, Davy SK. 2016. Metabolite profiling of symbiont and host during thermal stress and bleaching in a model cnidarian–dinoflagellate symbiosis. J Exp Biol. 219(4):516-527. https://doi.org/10.1242/jeb.128660 DOI: https://doi.org/10.1242/jeb.128660

Hou J, Xu T, Su D, Wu Y, Cheng L, Wang J, Zhou Z, Wang Y. 2018. RNA-Seq reveals extensive transcriptional response to heat stress in the stony coral Galaxea fascicularis. Front Genet. 9:37. https://doi.org/10.3389/fgene.2018.00037 DOI: https://doi.org/10.3389/fgene.2018.00037

Huang Y, Yuan J, Zhang Y, Peng H, Liu L. 2018. Molecular cloning and characterization of calmodulin-like protein CaLP from the Scleractinian coral Galaxea astreata. Cell Stress Chaperon. 23(6):1329-1335. https://doi.org/10.1007/s12192-018-0907-0 DOI: https://doi.org/10.1007/s12192-018-0907-0

Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, et al. 2018. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science. 359(6371):80-83. https://doi.org/10.1126/science.aan8048 DOI: https://doi.org/10.1126/science.aan8048

Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W. 2008. A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc Royal Soc B Biol Sci. 275:1359-1365. https://doi.org/10.1098/rspb.2008.0069 DOI: https://doi.org/10.1098/rspb.2008.0069

Kemp DW, Hernandez-Pech X, Iglesias-Prieto R, Fitt WK, Schmidt GW. 2014. Community dynamics and physiology of Symbiodinium spp. before, during, and after a coral bleaching event. Limnol Oceanogr. 59(3):788-797. https://doi.org/10.4319/lo.2014.59.3.0788 DOI: https://doi.org/10.4319/lo.2014.59.3.0788

Kennedy EV, Foster NL, Mumby PJ, Stevens JR. 2015. Widespread prevalence of cryptic Symbiodinium D in the key Caribbean reef builder, Orbicella annularis. Coral Reefs. 34:519-531. https://doi.org/10.1007/s00338-015-1264-4 DOI: https://doi.org/10.1007/s00338-015-1264-4

LaJeunesse TC. 2002. Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol. 141:387-400. https://doi.org/10.1007/s00227-002-0829-2 DOI: https://doi.org/10.1007/s00227-002-0829-2

LaJeunesse TC. 2004. “Species” radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol. 22(3):570-581. https://doi.org/10.1093/molbev/msi042 DOI: https://doi.org/10.1093/molbev/msi042

LaJeunesse TC, Smith RT, Finney J, Oxenford H. 2009. Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral ‘bleaching’ event. Proc Royal Soc B Biol Sci. 276:4139-4148. https://doi.org/10.1098/rspb.2009.1405 DOI: https://doi.org/10.1098/rspb.2009.1405

Le Tissier MDA. 1990. The ultrastructure of the skeleton and skeletogenic tissues of the temperate coral Caryophyllia smithii. J Mar Biol Assoc UK. 70(2):295-310. https://doi.org/10.1017/S0025315400035414 DOI: https://doi.org/10.1017/S0025315400035414

Le Tissier MDA. 1991. The nature of the skeleton and skeletogenic tissues in the Cnidaria. Hydrobiologia. 216(1):397-402. https://doi.org/10.1007/BF00026492 DOI: https://doi.org/10.1007/BF00026492

Levas S, Grottoli AG, Schoepf V, Aschaffenburg M, Baumann J, Bauer JE, Warner ME. 2016. Can heterotrophic uptake of dissolved organic carbon and zooplankton mitigate carbon budget deficits in annually bleached corals? Coral Reefs. 35:495-506. https://doi.org/10.1007/s00338-015-1390-z DOI: https://doi.org/10.1007/s00338-015-1390-z

Levas S, Schoepf V, Warner ME, Aschaffenburg M, Baumann J, Grottoli AG. 2018. Long-term recovery of Caribbean corals from bleaching. J Exp Mar Biol Ecol. 506:124-134. https://doi.org/10.1016/j.jembe.2018.06.003 DOI: https://doi.org/10.1016/j.jembe.2018.06.003

Lough JM, Anderson KD, Hughes TP. 2018. Increasing thermal stress for tropical coral reefs: 1871–2017. Sci Rep. 8:6079. https://doi.org/10.1038/s41598-018-24530-9 DOI: https://doi.org/10.1038/s41598-018-24530-9

Marshall PA, Baird AH. 2000. Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs. 19:155-163. https://doi.org/10.1007/s003380000086 DOI: https://doi.org/10.1007/s003380000086

Mayfield AB, Chen YJ, Lu CY, Chen CS. 2018. The proteomic response of the reef coral Pocillopora acuta to experimentally elevated temperatures. Plos one. 13:e0192001. https://doi.org/10.1371/journal.pone.0192001 DOI: https://doi.org/10.1371/journal.pone.0192001

McLachlan RH, Price JT, Solomon SL, Grottoli AG. 2020. Thirty years of coral heat-stress experiments: a review of methods. Coral Reefs. 39:885-902. https://doi.org/10.1007/s00338-020-01931-9 DOI: https://doi.org/10.1007/s00338-020-01931-9

Mieog JC, van Oppen MJH, Cantin NE, Stam WT, Olsen JL. 2007. Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian corals across the Great Barrier Reef: implications for symbiont shuffling. Coral Reefs. 26:449-457. https://doi.org/10.1007/s00338-007-0244-8 DOI: https://doi.org/10.1007/s00338-007-0244-8

Moya A, Ganot P, Furla P, Sabourault C. 2012. The transcriptomic response to thermal stress is immediate, transient and potentiated by ultraviolet radiation in the sea anemone Anemonia viridis. Mol Ecol. 21(5):1158-1174. https://doi.org/10.1111/j.1365-294X.2012.05458.x DOI: https://doi.org/10.1111/j.1365-294X.2012.05458.x

Muller-Parker G, D’Elia CF, Cook CB. 2015. Interactions between corals and their symbiotic algae. In: Birkeland C (ed.), Coral Reefs in the Anthropocene. Dordrecht (Netherlands): Springer. p. 99-116. https://doi.org/10.1007/978-94-017-7249-5_5 DOI: https://doi.org/10.1007/978-94-017-7249-5_5

Oakley CA, Durand E, Wilkinson SP, Peng L, Weis VM, Grossman AR, Davy SK. 2017. Thermal shock induces host proteostasis disruption and endoplasmic reticulum stress in the model symbiotic cnidarian Aiptasia. J Proteome Res. 16(6):2121-2134. https://doi.org/10.1021/acs.jproteome.6b00797 DOI: https://doi.org/10.1021/acs.jproteome.6b00797

Olguín-López N. Hérnandez-Elizárraga VH, Hernández-Matehuala R, Cruz-Hernández A, Guevara-González R, Caballero-Pérez J, Ibarra-Alvarado C, Rojas-Molina A. 2019. Impact of El Niño-Southern Oscillation 2015-2016 on the soluble proteomic profile and cytolytic activity of Millepora alcicornis (“fire coral”) from the Mexican Caribbean. PeerJ Aquat Biol. 7:e6593. https://doi.org/10.7717/peerj.6593/supp-1 DOI: https://doi.org/10.7717/peerj.6593

Oliver JK, Berkelmans R, Eakin CM. 2009. Coral bleaching in space and time. In: van Oppen MJH, Lough JM (eds.), Coral Bleaching. Berlin, Heidelberg (Germany): Springer. p. 21-39. https://doi.org/10.1007/978-3-540-69775-6_3 DOI: https://doi.org/10.1007/978-3-540-69775-6_3

Oliver TA, Palumbi SR. 2011. Many corals host thermally resistant symbionts in high-temperature habitat. Coral Reefs. 30:241-250. https://doi.org/10.1007/s00338-010-0696-0 DOI: https://doi.org/10.1007/s00338-010-0696-0

Pereira-Dias TL, Gondim AI. 2016. Bleaching in scleractinians, hydrocorals, and octocorals during thermal stress in a northeastern Brazilian reef. Mar Biodivers. 46:303-307. https://doi.org/10.1007/s12526-015-0342-8 DOI: https://doi.org/10.1007/s12526-015-0342-8

Reynolds JM, Bruns BU, Fitt WK, Schmidt GW. 2008. Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. PNAS. 105(36):13674-13678. https://doi.org/10.1073/pnas.0805187105 DOI: https://doi.org/10.1073/pnas.0805187105

Ricaurte M, Schizas NV, Ciborowski P, Boukli NM. 2016. Proteomic analysis of bleached and unbleached Acropora palmata, a threatened coral species of the Caribbean. Mar Poll Bull. 107(1):224-232. https://doi.org/10.1016/j.marpolbul.2016.03.068 DOI: https://doi.org/10.1016/j.marpolbul.2016.03.068

Rodriguez‐Lanetty M, Harii S, Hoegh‐Guldberg O. 2009. Early molecular responses of coral larvae to hyperthermal stress. Mol Ecol. 18(24):5101-5114. https://doi.org/10.1111/j.1365-294X.2009.04419.x DOI: https://doi.org/10.1111/j.1365-294X.2009.04419.x

Rodríguez L, López C, Casado-Amezua P, Ruiz-Ramos DV, Martínez B, Banaszak A, Tuya F, García-Fernández A, Hernández M. 2019. Genetic relationships of the hydrocoral Millepora alcicornis and its symbionts within and between locations across the Atlantic. Coral Reefs. 38:255-268. https://doi.org/10.1007/s00338-019-01772-1 DOI: https://doi.org/10.1007/s00338-019-01772-1

Rojas-Molina A, García-Arredondo A, Ibarra-Alvarado C, Bah MM. 2012. Millepora (“fire corals”) species: toxinological studies until 2011. Adv Env Res. 26:133-48.

Ruiz-Jones LJ, Palumbi SR. 2017. Tidal heat pulses on a reef trigger a fine-tuned transcriptional response in corals to maintain homeostasis. Sci Adv. 3(3):e1601298. https://doi.org/10.1126/sciadv.1601298 DOI: https://doi.org/10.1126/sciadv.1601298

Salgado A, Vieiralves T, Lamarão FR, Assumpção LL, Gomes D, Jascone L, Valadão AL, Albano RM, Lôbo-Hajdu G. 2007. Field preservation and optimization of a DNA extraction method for Porifera. In: Custodio MR, LôboHajdu G, Hajdu E, Muricy G (eds.), Porifera research: biodiversity, innovation and sustainability. Rio de Janeiro (Brazil): Série Livros 28, Museu Nacional. p. 555-560.

Sampayo EM, Ridgway T, Bongaerts P, Hoegh-Guldberg O. 2008. Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. PNAS. 105(30):10444-10449. https://doi.org/10.1073/pnas.0708049105 DOI: https://doi.org/10.1073/pnas.0708049105

Santos SR, Shearer TL, Hannes AR, Coffroth MA. 2004. Fine-scale diversity and specificity in the most prevalent lineage of symbiotic dinoflagellates (Symbiodinium, Dinophyceae) of the Caribbean. Mol Ecol. 13(2):459-469. https://doi.org/10.1046/j.1365-294x.2003.02058.x DOI: https://doi.org/10.1046/j.1365-294X.2003.02058.x

Schoepf V, Grottoli AG, Levas SJ, Aschaffenburg MD, Baumann JH, Matsui Y, Warner ME. 2015. Annual coral bleaching and the long-term recovery capacity of coral. Proc R Soc B. 282:20151887. https://doi.org/10.1098/rspb.2015.1887 DOI: https://doi.org/10.1098/rspb.2015.1887

Shirur KP, Ramsby BD, Iglesias-Prieto R, Goulet TL. 2014. Biochemical composition of Caribbean gorgonians: Implications for gorgonian — Symbiodinium symbiosis and ecology. J Exp Mar Biol Ecol. 461:275-285. https://doi.org/10.1016/j.jembe.2014.08.016 DOI: https://doi.org/10.1016/j.jembe.2014.08.016

Silverstein RN, Cunning R, Baker AC. 2015. Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Glob Chang Biol. 21(1):236-249. https://doi.org/10.1111/gcb.12706 DOI: https://doi.org/10.1111/gcb.12706

Suggett DJ, Smith DJ. 2020. Coral bleaching patterns are the outcome of complex biological and environmental networking. Glob Chang Biol. 26(1):68-79. https://doi.org/10.1111/gcb.14871 DOI: https://doi.org/10.1111/gcb.14871

Swain TD, Westneat MW, Backman V, Marcelino LA. 2018. Phylogenetic analysis of symbiont transmission mechanisms reveal evolutionary patterns in thermotolerance and host specificity that enhance bleaching resistance among vertically transmitted Symbiodinium. Eur J Phycol. 53(4):443-459. https://doi.org/10.1080/09670262.2018.1466200 DOI: https://doi.org/10.1080/09670262.2018.1466200

Tambutté E, Tambutté S, Segonds N, Zoccola D, Venn A, Erez J, Allemand D. 2012. Calcein labelling and electrophysiology: insights on coral tissue permeability and calcification. Proc Royal Soc B Biol Sci. 279:19-27. https://doi.org/10.1098/rspb.2011.0733 DOI: https://doi.org/10.1098/rspb.2011.0733

Tremblay P, Gori A, Maguer JF, Hoogenboom M, Ferrier-Pagès C. 2016. Heterotrophy promotes the re-establishment of photosynthate translocation in a symbiotic coral after heat stress. Sci Rep. 6:srep38112. https://doi.org/10.1038/srep38112 DOI: https://doi.org/10.1038/srep38112

Venn AA, Loram JE, Douglas AE. 2008. Photosynthetic symbioses in animals. J Exp Bot. 59(5):1069-1080. https://doi.org/10.1093/jxb/erm328 DOI: https://doi.org/10.1093/jxb/erm328

Wagner DE, Kramer P, van Woesik R. 2010. Species composition, habitat, and water quality influence coral bleaching in southern Florida. Mar Ecol Prog Ser. 408:65-78. https://doi.org/10.3354/meps08584 DOI: https://doi.org/10.3354/meps08584

Yellowlees D, Rees TAV, Leggat W. 2008. Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ. 31(5):679-694. https://doi.org/10.1111/j.1365-3040.2008.01802.x DOI: https://doi.org/10.1111/j.1365-3040.2008.01802.x