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Cryopreservation of sperm from the brain coral Diploria labyrinthiformis as a strategy to face the loss of corals in the Caribbean

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Abstract

In this study, we evaluated the efficacy of sperm cryopreservation for use in larval-based propagation of Diploria labyrinthiformis and produced offspring that were maintained under controlled conditions. Gametes were collected from colonies in situ in July and August 2017 and 2018. The four largest colonies out of a total of nine appear to be senescent or produce low-quality sperm or eggs. Sperm was cryopreserved for comparison of the effects of storage time on sperm viability. We determined that cryopreserved sperm from D. labyrinthiformis is viable for at least 13 months for use in in vitro crosses, though their motility is reduced on average by 24% in comparison with fresh sperm. Using frozen sperm to fertilize freshly collected eggs led to successful fertilization, larval yields, settlement and post-settlement survival. In general, these were lower by 23%, 23%, 14% and 8%, respectively, when compared to controls fertilized with fresh sperm. Our results suggest that motility of fresh sperm is not a good indicator of the future fate of larvae because in some cases low motility led to successful settlement. We also found that not all crosses were successful, and that the direction of the cross significantly affects larval yields and settlement. Once symbionts were noticeable within the primary polyps the cryo-recruits were maintained in an ex situ nursery for observation and showed similar survival with respect to recruits produced with fresh sperm. Prior to the 2018 spawning event, Stony Coral Tissue Loss Disease (SCTLD) was detected in the studied colonies and by February 2020 seven of the nine colonies (78%) had succumbed to the disease. The sperm from these colonies was banked in a repository and since then has been used in genetic rescue projects for this species. Thus, we show that cryopreservation is a useful tool in actions designed to recover D. labyrinthiformis and can potentially be applied to other species of corals severely affected by SCTLD or in need of genetic rescue.

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References

  • Alvarado-Chaparro E, Garcia R, Acosta A (2004) Sexual reproduction of the reef-building coral Diploria labyrinthiformis (Scleractinia:Faviidae) in the Colombian Caribbean. Rev Biol Trop 52:859–868

    Google Scholar 

  • Álvarez-Filip L, Estrada-Saldívar N, Pérez-Cervantes E, Molina-Hernández A, González-Barrios FJ (2019) A rapid spread of the stony coral tissue loss disease outbreak in the Mexican Caribbean. PeerJ 7:e8069

    Article  PubMed  PubMed Central  Google Scholar 

  • Barfield S, Aglyamova GV, Matz MV (2016) Evolutionary origins of germline segregation in Metazoa: evidence for a germ stem cell lineage in the coral Orbicella faveolata (Cnidaria, Anthozoa). Proc Biol Sci 83:20152128

    Google Scholar 

  • Baums IB, Devlin-Duarte MK, Polato NR, Xu D, Giri S, Altman NS, Ruiz D, Parkinson JE, Boulay JN (2013) Genotypic variation influences reproductive success and thermal stress tolerance in the reef building coral Acropora palmata. Coral Reefs 32:703–717

    Article  Google Scholar 

  • Carlson SM, Cunningham CJ, Westley PAH (2014) Evolutionary rescue in a changing world. Trends Ecol Evol 29:521–530

    Article  PubMed  Google Scholar 

  • Chamberland VF, Snowden S, Marhaver KL, Petersen D, Vermeij MJA (2017) The reproductive biology and early life ecology of a common Caribbean brain coral, Diploria labyrinthiformis (Scleractinia: Faviinae). Coral Reefs 36:83–94

    Article  Google Scholar 

  • Cirino L, Wen ZH, Hsieh K, Huang CL, Leong QL, Wang LH, Chen CS, Daly J, Tsai S, Lin C (2019) First instance of settlement by cryopreserved coral larvae in symbiotic association with dinoflagellates. Sci Rep 9:18851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daly J, Zuchowicz N, Nuñez Lendo CI, Khosla K, Lager C, Henley EM, Bischof J, Kleinhans FW, Lin C, Peters EC, Hagedorn M (2018) Successful cryopreservation of coral larvae using vitrification and laser warming. Sci Rep 8:15714

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Darling ES, Côté IM (2018) Seeking resilience in marine ecosystems. Science 359:986–987

    Article  CAS  PubMed  Google Scholar 

  • Fadlallah YH (1983) Sexual reproduction, development and larval biology in scleractinian corals: a review. Coral Reefs 2:129–150

    Article  Google Scholar 

  • Feuillassier L, Masanet P, Romans P, Barthélémy D, Engelmann F (2015) Towards a vitrification-based cryopreservation protocol for the coral Pocillopora damicornis L.: tolerance of tissue balls to 4.5M cryoprotectant solutions. Cryobiology 71:224–235

    Article  CAS  PubMed  Google Scholar 

  • Glassom D, Celleirs L, Schleyer MH (2006) Coral recruitment patterns at Sodwana Bay, South Africa. Coral Reefs 25:485–492

    Article  Google Scholar 

  • Häder D-P, Banaszak AT, Villafañe VE, Narvarte MA, González RA, Helbling EW (2020) Anthropogenic pollution of aquatic ecosystems: emerging problems with global implications. Sci Total Environ 713:136586

    Article  PubMed  CAS  Google Scholar 

  • Hagedorn M, Spindler R (2014) The reality, use and potential for cryopreservation of coral reefs. Adv Exp Med Biol 753:317–329

    Article  PubMed  Google Scholar 

  • Hagedorn M, Carter V (2016) Cryobiology: principles, species conservation and benefits for coral reefs. Reprod Fertil Dev 28:1049–1060

    Article  Google Scholar 

  • Hagedorn M, Spindler R, Daly J (2019) Cryopreservation as a tool for reef restoration. Adv Exp Med Biol 1200:489–505

    Article  PubMed  Google Scholar 

  • Hagedorn M, Pana R, Cox EF, Hollingsworth L, Krupp D, Lewis TD, Leong JC, Mazur P, Rall WF, MacFarlane DR, Fahy G, Kleinhans FW (2006) Coral larvae conservation: physiology and reproduction. Cryobiology 52:33–47

    Article  CAS  PubMed  Google Scholar 

  • Hagedorn M, Carter V, Martorana K, Paresa MK, Acker J, Baums IB, Borneman E, Brittsan M, Byers M, Henley M, Laterveer M, Leong J-A, McCarthy M, Meyers S, Nelson BD, Petersen D, Tiersch T, Cuevas Uribe R, Woods E, Wildt D (2012a) Preserving and using germplasm and dissociated embryonic cells for conserving Caribbean and Pacific coral. PLoS ONE 7:e33354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hagedorn M, Van OppenCarter MJHV, Henley M, Abrego D, Puill-Stephan E, Negri A, Heyward A, MacFarlane D, Spindler R (2012b) First frozen repository for the great barrier reef coral created. Cryobiology 65:157–158

    Article  PubMed  Google Scholar 

  • Hagedorn M, Farrell A, Carter VL (2013) Cryobiology of coral fragments. Cryobiology 66:17–23

    Article  CAS  PubMed  Google Scholar 

  • Hagedorn M, Carter VL, Henley EM, van Oppen MJH, Hobbs R, Spindler RE (2017) Producing coral offspring with cryopreserved sperm: a tool for coral reef restoration. Sci Rep 7:14432

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann AA, Sgrò CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485

    Article  CAS  PubMed  Google Scholar 

  • Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nyström M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    Article  CAS  PubMed  Google Scholar 

  • Lin C, Tsai S (2012) The effect of chilling and cryoprotectants on hard coral (Echinopora) oocytes during short-term low temperature preservation. Theriogenology 77:1257–1261

    Article  CAS  PubMed  Google Scholar 

  • Lin C, Wang LH, Fan TY, Kuo FW (2012) Lipid content and composition during the oocyte development of two gorgonian coral species in relation to low temperature preservation. PLoS ONE 7:e38689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McField M, Kramer P, Giró Petersen A, Soto M, Drysdale I, Craig N, Rueda Flores M (2020) 2020 Mesoamerican Reef Report Card, p 36

  • Muller E, Vermeij MJA (2011) Day time spawning of a Caribbean coral. Coral Reefs 30:1147

    Article  Google Scholar 

  • Novak BJ, Fraser D, Maloney TH (2020) Transforming ocean conservation: applying the genetic rescue toolkit. Genes 11:209

    Article  CAS  PubMed Central  Google Scholar 

  • Perry CT, Murphy GN, Kench PS, Smithers SG, Edinger EN, Steneck RS, Mumby PJ (2013) Caribbean-wide decline in carbonate production threatens coral reef growth. Nat Commun 4:1402

    Article  PubMed  CAS  Google Scholar 

  • Precht WF, Gintert BE, Robbart ML, Fura R, van Woesik R (2016) Unprecedented disease-related coral mortality in Southeastern Florida. Sci Rep 6:31374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shikina S, Chen CJ, Liou JY, Shao ZF, Chung YJ, Lee YH, Chang FC (2012) Germ cell development in the scleractinian coral Euphyllia ancora (Cnidaria, Anthozoa). PLoS ONE 7:e41569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shikina S, Chung YJ, Wang HM, Chiu YL, Shao ZF, Lee YH, Chang CF (2015) Immunohistochemical localization of early germ cells in a stony coral, Euphyllia ancora: potential implications for a germline stem cell system in coral gametogenesis. Coral Reefs 34:639–653

    Article  Google Scholar 

  • Tan ES, Izumi R, Takeuchi Y, Isomura N, Takemura A (2020) Molecular approaches underlying the oogenic cycle of the scleractinian coral, Acroporatenuis. Sci Rep 10:9914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsai S, Yang V, Lin C (2016) Comparison of the cryo-tolerance of vitrified gorgonian oocytes. Sci Rep 6:23290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsai S, Yen W, Chavanich S, Viyakarn V, Lin C (2015) Development of cryopreservation techniques for gorgonian (Junceella juncea) oocytes through vitrification. PLoS ONE 10:e0123409

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van Oppen MJ, Gates RD (2006) Conservation genetics and the resilience of reef-building corals. Mol Ecol 15:3863–3883

    Article  CAS  Google Scholar 

  • Van Oppen MJH, Oliver JK, Putnam HM, Gates RD (2015) Building coral reef resilience through assisted evolution. Proc Natl Acad Sci USA 112:2307–2313

  • Van Tussenbroek BI, Hernández Arana HA, Rodríguez-Martínez RE, Espinoza-Avalos J, Canizales-Flores HM, González-Godoy CE, Barba-Santos MG, Vega-Zepeda A, Collado-Vides L (2017) Severe impacts of brown tides caused by Sargassum spp. on near-shore Caribbean seagrass communities. Mar Pollut Bull 122:272–281

    Article  CAS  Google Scholar 

  • Viyakarn V, Chavanich S, Chong G, Tsai S, Lin C (2018) Cryopreservation of sperm from the coral Acropora humilis. Cryobiology 80:130–138

    Article  CAS  PubMed  Google Scholar 

  • Webster MS, Colton MA, Darling ES, Armstrong J, Pinsky ML, Knowlton N, Schindler DE (2017) Who should pick the winners of climate change? Trends Ecol Evol 32:167–173

    Article  PubMed  Google Scholar 

  • Weil E, Vargas WL (2010) Comparative aspects of sexual reproduction in the Caribbean coral genus Diploria (Scleractinia: Faviidae). Mar Biol 157:413–426

    Article  Google Scholar 

  • Wyers SC, Barnes HS, Smith SR (1991) Spawning of hermatypic corals in Bermuda: a pilot study. Hydrobiologia 216(217):109–116

    Article  Google Scholar 

  • Zhang Y, Chiu Y, Chen C, Ho Y, Shinzato C, Shikina S, Chang C (2019) Discovery of a receptor guanylate cyclase expressed in the sperm flagella of stony corals. Sci Rep 9:14652

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

This project was funded by CONACYT project number 247765 to ATB and EM. We sincerely appreciate the technical assistance of C. Morera Román, F. Negrete Soto, E. Escalante Mancera, M.A. Gómez Reali and R. Tecalco Rentería and the opportunity to learn cryopreservation techniques from Dr. Mary Hagedorn. We also wish to thank Dr. Hagedorn and two anonymous reviewers whose suggestions helped to improve the manuscript. This work was undertaken with a permit authorized by the National Aquaculture and Fisheries Commission (CONAPESCA Nº. PPF/DGOPA-003/2017).

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Authors and Affiliations

  1. Integrative Reef Conservation Research Laboratory, Instituto de Ciencias del Mar y Limnología, Unidad Académica de Sistemas Arrecifales, Universidad Nacional Autónoma de México, Puerto Morelos, Quintana Roo, Mexico

    M. V. Grosso-Becerra, S. Mendoza-Quiroz & A. T. Banaszak

  2. SECORE International, Inc, Hilliard, OH, USA

    S. Mendoza-Quiroz

  3. EvoDevo Research Group, Instituto de Ciencias del Mar y Limnología, Unidad Académica de Sistemas Arrecifales, Universidad Nacional Autónoma de México, Puerto Morelos, Quintana Roo, Mexico

    M. V. Grosso-Becerra & E. Maldonado

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  1. M. V. Grosso-Becerra
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  4. A. T. Banaszak
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Grosso-Becerra, M.V., Mendoza-Quiroz, S., Maldonado, E. et al. Cryopreservation of sperm from the brain coral Diploria labyrinthiformis as a strategy to face the loss of corals in the Caribbean. Coral Reefs 40, 937–950 (2021). https://doi.org/10.1007/s00338-021-02098-7

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