Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH FRONT (Open Access)

Potential bleaching effects on coral reproduction

Mary Hagedorn A B C , Virginia L. Carter A B , Claire Lager B , Julio F. Camperio Ciani A B , Alison N. Dygert A B , Reuben D. Schleiger A B and E. Michael Henley A B

A Department of Reproductive Sciences, Smithsonian Conservation Biology Institute – National Zoological Park, Front Royal, VA 22630, USA.

B Hawai’i Institute of Marine Biology, University of Hawaii, Kaneohe, HI 96744, USA.

C Corresponding author. Email: hagedornm@si.edu

Reproduction, Fertility and Development 28(8) 1061-1071 https://doi.org/10.1071/RD15526
Submitted: 12 December 2015  Accepted: 5 April 2016   Published: 17 June 2016

Abstract

Bleaching profoundly impacts coral reproduction, often for years after an event. However, detailed reproductive characteristics of coral after bleaching have not been broadly described, especially as they relate to cryopreservation. Therefore, in the present study we measured several reproductive characteristics in coral in Kaneohe Bay, Hawaii, for two species, namely Fungia scutaria and Montipora capitata, during the bleaching period of 2014 and 2015. We examined spawning periods, egg morphometry, sperm concentration, fresh and cryopreserved sperm motility exposed to different concentrations of dimethyl sulfoxide, time of first cleavage, larval survival with fresh and cryopreserved spermatozoa, infection success and settlement success. Many of these reproductive parameters were reduced in 2015, especially sperm motility. Once the reduced-motility spermatozoa from 2015 post-bleach were cryopreserved, there was a steep decline in post-thaw viability and this would prevent any substantive further use of these samples in reproduction for conservation benefit. Worldwide, as bleaching events become more frequent, the ability to bank and conserve coral ex situ may be significantly reduced. Thus, it is imperative that while genetic diversity is still high in these populations, intensive efforts are made to bank coral species during non-bleaching periods.

Additional keywords: cryopreservation, Fungia scutaria, Montipora capitata, sperm, Symbiodinium.


References

Anthony, K. R. N., Hoogenboom, M. O., Maynard, J. F., Grottoli, A. G., and Middlebrook, R. (2009). Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Funct. Ecol. 23, 539–550.
Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching.CrossRef | open url image1

Bahr, K. D., Jokiel, P. L., and Toonen, R. J. (2015). The unnatural history of Kāne’ohe Bay: coral reef resilience in the face of centuries of anthropogenic impacts. PeerJ 3, e950.
The unnatural history of Kāne’ohe Bay: coral reef resilience in the face of centuries of anthropogenic impacts.CrossRef | 26020007PubMed | open url image1

Baker, A. C. (2003). Flexibility and specificity in coral–algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu. Rev. Ecol. Evol. Syst. 34, 661–689.
Flexibility and specificity in coral–algal symbiosis: diversity, ecology, and biogeography of Symbiodinium.CrossRef | open url image1

Baker, A. C., Glynn, P. W., and Riegl, B. (2008). Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar. Coast. Shelf Sci. 80, 435–471.
Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook.CrossRef | open url image1

Cox, E. F. (2007). Continuation of sexual reproduction in Montipora capitata following bleaching. Coral Reefs 26, 721–724.
Continuation of sexual reproduction in Montipora capitata following bleaching.CrossRef | open url image1

Cox, E. F., and Ward, S. (2002). Impact of elevated ammonium on reproduction in two Hawaiian scleractinian corals with different life history patterns. Mar. Pollut. Bull. 44, 1230–1235.
Impact of elevated ammonium on reproduction in two Hawaiian scleractinian corals with different life history patterns.CrossRef | 1:CAS:528:DC%2BD38XovFeiur4%3D&md5=83036450cb016fea54ebc9e6ac6d7894CAS | 12523521PubMed | open url image1

Ferrier-Pagès, C., Richard, C., Forcioli, D., Allemand, D., Pichon, M., and Shick, J. M. (2007). Effects of temperature and UV radiation increases on the photosynthetic efficiency in four scleractinian coral species. Biol. Bull. 213, 76–87.
Effects of temperature and UV radiation increases on the photosynthetic efficiency in four scleractinian coral species.CrossRef | 17679722PubMed | open url image1

Field, S. (1998) Settlement Biology of Larvae of Montipora verrucosa and Porites lobata in Hawaii. In: ‘Reproduction in Reef Corals Results of the 1997 Edwin W. Pauley Summer Program in Marine Biology, Technical report No. 42’. (Eds E. F. Cox, D. A. Krupp, P. L. Jokiel) pp. 111–119. (University of Hawaii: Honolulu.)

Fitt, K., Brown, B. E., Warner, M. E., and Dunne, R. P. (2001). Coral bleaching interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20, 51–65.
Coral bleaching interpretation of thermal tolerance limits and thermal thresholds in tropical corals.CrossRef | open url image1

Glynn, P. W. (1991). Coral reef bleaching in the 1980s and possible connections with global warming. Trends Ecol. Evol. 6, 175–179.
Coral reef bleaching in the 1980s and possible connections with global warming.CrossRef | 1:STN:280:DC%2BC3M7hsVegtw%3D%3D&md5=3675aa344053b98e92a3139cb713722eCAS | 21232450PubMed | open url image1

Glynn, P. W. (1993). Coral reef bleaching: ecological perspectives. Coral Reefs 12, 1–17.
Coral reef bleaching: ecological perspectives.CrossRef | open url image1

Glynn, P. W. (1996). Coral reef bleaching: facts, hypotheses and implications. Glob. Change Biol. 2, 495–509.
Coral reef bleaching: facts, hypotheses and implications.CrossRef | open url image1

Glynn, P. W., and D’Crox, L. (1990). Experimental evidence for high temperature stress as the cause of El Niño-coincident coral mortality. Coral Reefs 8, 181–191.
Experimental evidence for high temperature stress as the cause of El Niño-coincident coral mortality.CrossRef | open url image1

Goreau, T. J. (1992). Bleaching and reef community change in Jamaica: 1951–1991. Am. Zool. 32, 683–695.
Bleaching and reef community change in Jamaica: 1951–1991.CrossRef | open url image1

Hagedorn, M., Pan, R., Cox, E. F., Hollingsworth, L., Krupp, D., Lewis, T. D., Leong, J. C., Mazur, P., Rall, W. F., MacFarlane, D. R., Fahy, G., and Kleinhans, F. W. (2006). Coral larvae conservation: physiology and reproduction. Cryobiology 52, 33–47.
Coral larvae conservation: physiology and reproduction.CrossRef | 1:STN:280:DC%2BD28%2FosFOgsw%3D%3D&md5=f973d8db01d574914abf49cc0510151bCAS | 16337183PubMed | open url image1

Hagedorn, M., Carter, V. L., Hollingsworth, L., Leong, J. C., Kanno, R., Borneman, E. H., Petersen, D., Laterveer, M., Brittsan, M., and Schick, M. (2009). Ex situ culture of Caribbean and Pacific coral larvae comparing various flow-through chambers. In ‘Proceedings of the Smithsonian Marine Science Symposium’. (Eds M. A. Lang, I. G. Macintyre, K. Rutzler) pp. 259–268. (Smithsonian Institution Press: Washington DC.)

Hagedorn, M., Carter, V. L., Ly, S., Andrell, R. M., Yancey, P. H., Leong, J. A., and Kleinhans, F. W. (2010). Analysis of internal osmolality in developing coral larvae, Fungia scutaria. Physiol. Biochem. Zool. 83, 157–166.
Analysis of internal osmolality in developing coral larvae, Fungia scutaria.CrossRef | 19938981PubMed | open url image1

Hagedorn, M., Carter, V., Martorana, K., Paresa, M. K., Acker, J., Baums, I. B., Borneman, E., Brittsan, M., Byers, M., Henley, M., Laterveer, M., Leong, J. A., McCarthy, M., Meyers, S., Nelson, B. D., Petersen, D., Tiersch, T., Uribe, R. C., Woods, E., and Wildt, D. (2012). Preserving and using germplasm and dissociated embryonic cells for conserving Caribbean and Pacific coral. PLoS One 7, e33354.
Preserving and using germplasm and dissociated embryonic cells for conserving Caribbean and Pacific coral.CrossRef | 1:CAS:528:DC%2BC38XktF2it7Y%3D&md5=af5f090fc61fe99829dea0d422c6a042CAS | 22413020PubMed | open url image1

Hagedorn, M., Carter, V., Zuchowicz, N., Phillips, M., Penfield, C., Shamenek, B., Vallen, E. A., Kleinhans, F. W., Peterson, K., White, M., and Yancey, P. H. (2015a). Trehalose is a chemical attractant in the establishment of coral symbiosis. PLoS One 10, e0117087.
Trehalose is a chemical attractant in the establishment of coral symbiosis.CrossRef | 25629699PubMed | open url image1

Hagedorn, M., Farrell, A., Carter, V., Zuchowicz, N., Johnston, E., Padilla-Gamino, J., Gunasekera, S., and Paul, V. (2015b). Effects of toxic compounds in Montipora capitata on exogenous and endogenous zooxanthellae performance and fertilization success. PLoS One 10, e0118364.
Effects of toxic compounds in Montipora capitata on exogenous and endogenous zooxanthellae performance and fertilization success.CrossRef | 25714606PubMed | open url image1

Intergovernment Panel on Climate Change (IPCC) (2007) Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. (Eds S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, M. Tignor, H. L. Miller.) (Cambridge University Press: Cambridge.)

Jokiel, P. L., and Brown, E. K. (2004). Global warming, regional trends and inshore environmental conditions influence coral bleaching in Hawaii. Glob. Change Biol. 10, 1627–1641.
Global warming, regional trends and inshore environmental conditions influence coral bleaching in Hawaii.CrossRef | open url image1

Jokiel, P. L., and Coles, S. L. (1990). Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral Reefs 8, 155–162.
Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature.CrossRef | open url image1

Kawaguti, S. (1944). On the physiology of reef corals VI. Study on the pigments. Palao Trop. Biol. Stn. Stud. 2, 617–674. open url image1

Krupp, D. A. (1983). Sexual reproduction and early development of the solitary coral Fungia scutaria (Anthozoa: Scleractinia). Coral Reefs 2, 159–164.
Sexual reproduction and early development of the solitary coral Fungia scutaria (Anthozoa: Scleractinia).CrossRef | open url image1

LaJeunesse, T. C., Thornhill, D. J., Cox, E. F., Stanton, F. G., Fitt, W. K., and Schmidt, G. W. (2004). High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23, 596–603. open url image1

Lesser, M. P., and Shick, M. J. (1989). Effects of irradiance and ultra-violet radiation on photoadaptation in the zooxanthellae of Aiptasia pallida:primary production, photoinhibition, and enzymatic defenses against oxygen toxicity. Mar. Biol. 102, 243–255.
Effects of irradiance and ultra-violet radiation on photoadaptation in the zooxanthellae of Aiptasia pallida:primary production, photoinhibition, and enzymatic defenses against oxygen toxicity.CrossRef | open url image1

Levitan, D. R., Boudreau, W., Jara, J., and Knowlton, N. (2014). Long-term reduced spawning in Orbicella coral species due to temperature stress. Mar. Ecol. Prog. Ser. 515, 1–10.
Long-term reduced spawning in Orbicella coral species due to temperature stress.CrossRef | open url image1

McLaughlin, J. J. A., and Zahl, P. A. (1959). Axenic Zooxanthellae from various invertebrate hosts. Ann. N. Y. Acad. Sci. 77, 55–72.
Axenic Zooxanthellae from various invertebrate hosts.CrossRef | open url image1

Nielson, B. (2014). ‘DAR Coral Bleaching Rapid Response Surveys September–October 2014.’ Available at http://dlnr.hawaii.gov/reefresponse/files/2014/10/DARCoralBleachingSrvy_Results_10.28.2014.pdf

Padilla-Gamiño, J. L., and Gates, R. D. (2012). Spawning dynamics in the Hawaiian reef-building coral Montipora capitata. Mar. Ecol. Prog. Ser. 449, 145–160.
Spawning dynamics in the Hawaiian reef-building coral Montipora capitata.CrossRef | open url image1

Padilla-Gamiño, J. L., Weatherby, T. M., Waller, R. G., and Gates, R. D. (2011). Formation and structural organization of the egg–sperm bundle of the scleractinian coral Montipora capitata. Coral Reefs 30, 371–380.
Formation and structural organization of the egg–sperm bundle of the scleractinian coral Montipora capitata.CrossRef | open url image1

Padilla-Gamiño, J. L., Hedouin, L., Waller, R. G., Smith, D., Truong, W., and Gates, R. D. (2014). Sedimentation and the reproductive biology of the Hawaiian reef-building coral Montipora capitata. Biol. Bull. 226, 8–18.
| 24648203PubMed | open url image1

Randall, C. J., and Szmant, A. M. (2009). Elevated temperature affects development, survivorship, and settlement of the elkhorn coral, Acropora palmata (Lamarck 1816). Biol. Bull. 217, 269–282.
| 20040751PubMed | open url image1

Relman, D. A. (2008). ‘Til death do us part’: coming to terms with symbiotic relationships. Nat. Rev. Microbiol. 6, 721–724.
‘Til death do us part’: coming to terms with symbiotic relationships.CrossRef | 1:CAS:528:DC%2BD1cXhtFWitL3M&md5=5eea378441c1e4ceb9894878bd990144CAS | 19086265PubMed | open url image1

Schoepf, V., Grottoli Aé, G., Warner, M. E., Cai, W. J., Melman, T. F., Hoadley, K. D., Pettay, D. T., Hu, X., Li, Q., Xu, H., Wang, Y., Matsui, Y., and Baumann, J. H. (2013). Coral energy reserves and calcification in a high-CO2 world at two temperatures. PLoS One 8, e75049.
Coral energy reserves and calcification in a high-CO2 world at two temperatures.CrossRef | 1:CAS:528:DC%2BC3sXhs1Cns7zM&md5=55824d3badc2f5ced4b483917a590000CAS | 24146747PubMed | open url image1

Schwarz, J. A., Krupp, D. A., and Weis, V. M. (1999). Late larval development and onset of symbiosis in the scleractinian coral Fungia scutaria. Biol. Bull. 196, 70–79.
Late larval development and onset of symbiosis in the scleractinian coral Fungia scutaria.CrossRef | 1:STN:280:DC%2BC2Mvls1OntA%3D%3D&md5=d135093880959ffbef894132996471ebCAS | 25575388PubMed | open url image1

Szmant, A. M., and Gassman, N. J. (1990). The effects of prolonged ‘bleaching’ on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 8, 217–224.
The effects of prolonged ‘bleaching’ on the tissue biomass and reproduction of the reef coral Montastrea annularis.CrossRef | open url image1

Vaughan, T. W. (1914). Sketch of the geologic history of the Florida coral reef tract and comparisons with other coral reef areas. J. Wash. Acad. Sci. 4, 26–34. open url image1

Vermeij, M. J., Smith, J. E., Smith, C. M., Vega Thurber, R., and Sandin, S. A. (2009). Survival and settlement success of coral planulae: independent and synergistic effects of macroalgae and microbes. Oecologia 159, 325–336.
Survival and settlement success of coral planulae: independent and synergistic effects of macroalgae and microbes.CrossRef | 1:STN:280:DC%2BD1M7ksVeiug%3D%3D&md5=25aed2dbabf660cce9093016381aeeebCAS | 19050932PubMed | open url image1

Ward, S., Harrison, P., and Hoegh-Guldberg, O. (2002) Coral bleaching reduces reproduction of scleractinian corals and increases susceptibility to future stress. In ‘Proceedings of the Ninth International Coral Reef Symposium’, Volume 2, 23–27 October 2000, Bali. (Eds M. K. Moosa, S. Soemodihardjo, A. Soegiarto, K. Romimohtarto, A. Nontji, S. Suharsono.) pp. 1123–1128. (Ministry of Environment, Indonesian Institute of Sciences, International Society for Reef Studies: Bali.)


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