Abstract
Bleaching events are becoming more frequent and intense worldwide. Southwestern Atlantic corals are considered stress-tolerant species that suffer less during bleaching episodes. Therefore, we investigated if the reef-building corals Mussismilia hispida and M. harttii are capable of spawning while fully bleached. We compared spermatozoa concentration and motility, egg diameter and embryo viability between seemingly healthy and bleached colonies for both species. Findings show that both species spawned viable gametes. Concentration and motility of newly-released spermatozoa were similar between healthy and bleached colonies for both species. Unlike M. hispida, a 10% reduction in size was found in egg diameter for M. harttii. Embryo viability for bleached M. hispida colonies did not decrease; for bleached M. harttii there was a reduction from 14.7 to 6.3%, but fertilization and larval development still took place. These findings describe the unprecedented episode of corals spawning viable gametes when entirely bleached, supporting the suggestion of greater resilience for Southwestern Atlantic corals.
Data availability
The data generated and analyzed during this study are available from the corresponding author upon request.
References
Anthony KRN, Fabricius KE (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J Exp Mar Biol Ecol 252:221–253. https://doi.org/10.1016/S0022-0981(00)00237-9
Armoza-Zvuloni R, Segal R, Kramarsky-Winter E, Loya Y (2011) Repeated bleaching events may result in high tolerance and notable gametogenesis in stony corals: Oculina patagonica as a model. Mar Ecol Prog Ser 426:149–159. https://doi.org/10.3354/meps09018
Banha TNS, Capel KCC, Kitahara MV, Francini-Filho RB, Francini CLB, Sumida PYG, Mies M (2020) Low coral mortality during the most intense bleaching event ever recorded in subtropical Southwestern Atlantic reefs. Coral Reefs 39:515–521. https://doi.org/10.1007/s00338-019-01856-y
Caldas JS, Godoy L (2019) Sperm characterization of the endangered Amazonian fish Hypancistrus zebra: basic knowledge for reproduction and conservation strategies. AnimReprod Sci 204:117–124. https://doi.org/10.1016/j.anireprosci.2019.03.012
Castro CB, Pires DO (2001) Brazilian coral reefs: what we already know and what is still missing. Bull Mar Sci 69:357–371
Cox EF (2007) Continuation of sexual reproduction in Montipora capitata following bleaching. Coral Reefs 26:721–724. https://doi.org/10.1007/s00338-007-0251-9
Dajka JC, Wilson SK, Robinson JPW, Chong-Seng KM, Harris A, Graham NAJ (2019) Uncovering drivers of juvenile coral density following mass bleaching. Coral Reefs 38:637–649. https://doi.org/10.1007/s00338-019-01785-w
De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27 year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci 109:17995–17999. https://doi.org/10.1073/pnas.1208909109
Eakin CM, Morgan JA, Heron SF, Smith TB, Liu G, Alvarez- Filip L, Baca B, Bartels E, Bastidas C, Bouchon C, Brandt M, Bruckner AW, Bunkley-Williams L, Cameron A, Causey B, Chiappone M, Christensen TRL, Crabbe MJC, Day O, de la Guardia E, Díaz-Pulido G, DiResta D, Gil-Agudelo D, Gilliam DS, Ginsburg RN, Gore S, Guzmán HM, Hendee JC, Hernández-Delgado EA, Husain E, Jeffrey CFG, Jones RJ, Jordán-Dahlgren E, Kaufman LS, Kline DI, Kramer PA, Lang JC, Lirman D, Mallela J, Manfrino C, Maréchal JP, Marks K, Mihaly J, Miller WJ, Mueller EM, Orozco Toro CA, Oxenford HA, Ponce-Taylor D, Quinn N, Ritchie KB, Rodríguez S, Rodríguez Ramírez A, Romano S, Samhouri JF, Sánchez JA, Schmahl GP, Shank BV, Skirving WJ, Steiner SCC, Villamizar E, Walsh SM, Walter C, Weil E, Williams EH, Woody Roberson K, Yusuf Y (2010) Caribbean corals in crisis: record thermal stress, bleaching, and mortality in 2005. PLoS ONE 5(11):e13969. https://doi.org/10.1371/journal.pone.0013969.g002
Fisch J, Drury C, Towle EK, Winter RN, Miller MW (2019) Physiological and reproductive repercussions of consecutive summer bleaching events of the threatened caribbean coral Orbicella faveolata. Coral Reefs 38:863–876. https://doi.org/10.1007/s00338-019-01817-5
Glynn PW (1993) Coral reef bleaching—ecological perspectives. Coral Reefs 12:1–17
Graham NAJ (2014) Habitat complexity: coral structural loss leads to fisheries declines. Curr Biol 24:R359–R361. https://doi.org/10.1016/j.cub.2014.03.069
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
Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189. https://doi.org/10.1038/nature04565
Hagedorn M, Carter VL, Lager C, Ciani JFC, Dygert AN, Schleiger RD, Henley M (2016) Potential bleaching effects on coral reproduction. ReprodFertil Dev 28:1061–1071. https://doi.org/10.1071/RD15526
Hancoch JL (1957) The morphology of boar spermatozoa. J R MicroscSoc 76:84–97. https://doi.org/10.1111/j.1365-2818.1956.tb00443.x
Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Ecosystems of the world: coral reefs, vol 25. Elsevier, New York, pp 133–207
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of world’s coral reefs. Mar Freshw Res 50:839–866. https://doi.org/10.1071/MF99078
Houlbrèque F, Ferrier-Pagès C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev Camb Philos Soc 84:1–17. https://doi.org/10.1111/j.1469-185X.2008.00058.x
Howells EJ, Ketchum RN, Bauman AG, Mustafa Y, Watkins KD, Burt JA (2016) Species-specific trends in the reproductive output of corals across environmental gradients and bleaching histories. Mar Pollut Bull 105:532–539. https://doi.org/10.1016/j.marpolbul.2015.11.034
Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250–2263. https://doi.org/10.1890/0012-9658(2000)081[2250:RFLHAL]2.0.CO;2
Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin CM, Gilmour JP, Graham NAJ, Harrison H, Hobbs J-PA, Hoey AS, Hoogenboom M, Lowe RJ, McCulloch MT, Pandolfi JM, Pratchett M, Schoepf V, Torda G, Wilson SK (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83. https://doi.org/10.1126/science.aan8048
Hughes TP, Kerry JT, Baird AH, Connolly SR, Chase TJ, Dietzel A, Hill T, Hoey AS, Hoogenboom MO, Jacobson M, Kerswell A, Madin JS, Mieog A, Paley AS, Pratchett MS, Torda G, Woods RM (2019) Global warming impairs stock–recruitment dynamics of corals. Nature 568:387–390. https://doi.org/10.1038/s41586-019-1081-y
Leão ZMAN, Kikuchi RKP, Oliveira MDM, Vasconcellos V (2010) Status of Eastern Brazilian coral reefs in time of climate changes. Pan-Am J Aquat Sci 5:224–235
Leão ZMAN, Kikuchi RKP, Ferreira BP, Neves EG, Sovierzoski HH, Oliveira MDM, Maida M, Correia MD, Johnsson R (2016) Brazilian coral reefs in a period of global change: a synthesis. Braz J Oceanogr 64:97–116. https://doi.org/10.1590/S1679-875920160916064sp2
Leggat WP, Camp EF, Suggett DJ, Heron SF, Fordyce AJ, Gardner S, Deakin L, Turner M, Beeching LJ, Kuzhiumparambil U, Eakin CM, Ainsworth TD (2019) Rapid coral decay is associated with marine heatwave mortality events on reefs. Curr Biol 29:2723–2730. https://doi.org/10.1016/j.cub.2019.06.077
Levitan DR, Boudreau W, Jara J, Knowlton N (2014) Long-term reduced spawning in Orbicella coral species due to temperature stress. Mar Ecol Prog Ser 515:1–10. https://doi.org/10.3354/meps11063
Liu G, Strong AE, Skirving WJ, Arzayus LF (2006) Overview of NOAA coral reef watch program’s near-real-time satellite global coral bleaching monitoring activities. In: Proceedings of 10th international coral reef symposium, 1:1783–1793
Marangoni LFB, Mies M, Güth AZ, Banha TNS, Inague A, Fonseca JS, Dalmolin C, Faria SC, Ferrier-Pagès C, Bianchini A (2019) Peroxynitrite generation and increased heterotrophic capacity are linked to the disruption of the coral-dinoflagellate symbiosis in scleractinian and hydrocoral species. Microorganisms 7:426. https://doi.org/10.3390/microorganisms7100426
Mendes JM, Woodley JD (2002) Effect of the 1995–1996 bleaching event on polyp tissue depth, growth, reproduction and skeletal band formation in Montastraea annularis. Mar Ecol Prog Ser 235:93–102
Mies M, Güth AZ, Castro CB, Pires DO, Calderon EN, Pompeu M, Sumida PYG (2018a) Bleaching in reef invertebrate larvae associated with Symbiodinium strains within clades A-F. Mar Biol 165:6. https://doi.org/10.1007/s00227-017-3263-1
Mies M, Guth AZ, Tenorio AA, Banha TNS, Waters L, Polito P, Taniguchi S, Bicego MC, Sumida PYG (2018b) In situ shifts of predominance between autotrophic and heterotrophic feeding in the reef-building coral Mussismilia hispida: an approach using fatty acid trophic markers. Coral Reefs 37:677–689. https://doi.org/10.1007/s00338-018-1692-z
Mies M, Francini-Filho RB, Zilberberg C, Garrido AG, Longo GO, Laurentino E, Güth AZ, Sumida PYG, Banha TNS (2020) South Atlantic are major global warming refugia and less susceptible to bleaching. Front Mar Sci. https://doi.org/10.3389/fmars.2020.00514
Moberg F, Folke C (1999) Ecological good and services of coral reef ecosystems. Ecol Econ 29:215–233. https://doi.org/10.1016/S0921-8009(99)00009-9
Neves EG, Pires DO (2002) Sexual reproduction of Brazilian coral Mussismilia hispida (Verrill, 1902). Coral Reefs 21:161–168. https://doi.org/10.1007/s00338-002-0217-x
Pereira-Filho GH, Shintate GSI, Kitahara MV, Moura RL, Amado-Filho GM, Bahia RG, Moraes FC, Neves LM, Francini CLB, Gibran FZ, Motta FS (2019) The southernmost Atlantic coral reef is off the subtropical island of Queimada Grande (24° S), Brazil. Bull Mar Sci 95:277–287. https://doi.org/10.5343/bms.2018.0056
Picciani N, de Lossio e Seiblitz IG, de Paiva PC, Castro CB, Zilberberg C (2016) Geographic patterns of Symbiodinium diversity associated with the coral Mussismilia hispida (Cnidaria, Scleractinia) correlate with major reef regions in the Southwestern Atlantic Ocean. Mar Biol 163:236. https://doi.org/10.1007/s00227-016-3010-z
Pires DO, Castro CB, Ratto CC (1999) Reef coral reproduction in the Abrolhos Reef Complex, Brazil: the endemic genus Mussismilia. Mar Biol 135:463–471. https://doi.org/10.1007/s002270050646
Pires DO, Castro CB, Segal B, Pereira CM, Carmo EC, Silva RG, Calderon EN (2016) Reprodução de corais de águas rasas do Brasil. In: Zilberberg C, Abrantes DP, Marques JÁ, Machado LF, Marangoni LFB (eds) Conhecendo os recifes brasileiros. Museu Nacional, Rio de Janeiro, pp 111–128
Ramirez-Llodra E (2002) Fecundity and life-history strategies in marine invertebrates. In: Advances in marine biology. Academic Press, pp 87–170
Rodríguez-Troncoso AP, Carpizo-Ituarte E, Leyte-Morales GE, Chi-Barragán G, Tapia-Vázquez O (2011) Sexual reproduction of three coral species from the Mexican South Pacific. Mar Biol 158:2673–2683. https://doi.org/10.1007/s00227-011-1765-9
Sakai Y, Hatta M, Furukawa S, Kawata M, Ueno N, Maruyama S (2020) Environmental factors explain spawning day deviation from full moon in the scleractinian coral Acropora. Biol Lett 16:6. https://doi.org/10.1098/rsbl.2019.0760
Shlesinger T, Loya Y (2019) Sexual reproduction of scleractinian corals in mesophotic coral ecosystems vs. shallow reefs. In: Loya Y, Puglise K, Bridge T (eds) Mesophotic coral ecosystems. Coral reefs of the world. Springer, Cha, pp 653–666. https://doi.org/10.1007/978-3-319-92735-0_35
Siebeck UE, Marshall NJ, Kluter A, Hoegh-Guldberg O (2006) Monitoring coral bleaching using a colour reference card. Coral Reefs 25:453–460. https://doi.org/10.1007/s00338-006-0123-8
Speare KE, Duran A, Miller MW, Burkepile DE (2019) Sediment associated with algal turfs inhibits the settlement of two endangered coral species. Mar Poll Bull 144:189–195
Suggett DJ, Smith DJ (2011) Interpreting the sign of coral bleaching as friend vs. foe. Glob Chang Biol 17:45–55. https://doi.org/10.1111/j.1365-2486.2009.02155.x
Szmant AM, Gassman NJ (1990) The effects of prolonged “bleaching” on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 8:217–224. https://doi.org/10.1007/BF00265014
Ward S, Harrison P, Hoegh-Guldberg O (2000) Coral bleaching reduces reproduction of scleractinian corals and increases susceptibility to future stress. In: Proc 8th Int Coral Reef Symp 2:1123–1128
Zar JH (1999) Biostatistical analysis. Prentice-Hall, Englewood Cliffs
Acknowledgements
The Coral Vivo Project and its sponsors, Petrobras, through the Petrobras Socioenvironmental Program, and Arraial d’Ajuda Eco Parque, are acknowledged for funding field research and use of research station facilities. We are grateful for the financial support from Boticário Group Foundation for Nature Protection (1138/2018-2). NC was granted a field-research scholarship from the Brazilian Biodiversity Fund (Funbio) and Instituto Humanize (N° 018/2019). LG is a research fellow from CNPq (310463/2018-1).
Author information
Authors and Affiliations
Contributions
LG, MM, YP and AA designed the study; LG, CZ, YP, AA, NC, CP, AGG and AP performed the experiments; LFAS and DOP contributed to infrastructure/material/technical support; YP, AA and AGG analyzed the data; and all authors contributed to the manuscript.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflict of interest.
Ethical approval
The authors declare that all applicable international, national and/or institutional guidelines for sampling, care and experimental use of animals for the study have been followed, and all necessary approvals by the Chico Mendes Institute for Biodiversity Conservation—ICMBio (SISBIO Nº 63368-1) have been obtained.
Additional information
Responsible Editor: S. Harii.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Reviewed by undisclosed experts.
Rights and permissions
About this article
Cite this article
Godoy, L., Mies, M., Zilberberg, C. et al. Southwestern Atlantic reef-building corals Mussismilia spp. are able to spawn while fully bleached. Mar Biol 168, 15 (2021). https://doi.org/10.1007/s00227-021-03824-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-021-03824-z