Variable PSII functioning and bleaching conditions of tropical scleractinian corals pre-and post-bleaching event
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Abstract. Mattan-Moorgawa S, Rughooputh SDDV, Bhagooli R. 2018. Variable PSII functioning and bleaching conditions of tropical scleractinian corals pre-and post-bleaching event. Ocean Life 1: 1-10. This study compared pre-bleaching and post-bleaching conditions of eight reef-building corals, Acropora cytherea, Acropora hyacynthus, Acropora muricata, Acropora sp., Pocillopora damicornis, Pocillopora eydouxi, Galaxea fascicularis and Fungia sp., in terms of visual coloration (non-bleached (NB), pale (P), partially bleached (PB) and bleached (B)) and chlorophyll fluorescence yield at photosystem II (PSII)). A total of twenty colonies from twelve stations along four transects were surveyed at Belle-Mare, Mauritius, from October 2008 to October 2009, and compared to the CoralWatch Coral Health Chart. PSII functioning, measured as Fv/Fm, were recorded in coral samples using a pulse-amplitude-modulated (PAM) fluorometer. Physico-chemical parameters (sea surface temperature, dissolved oxygen, salinity and pH) were recorded in situ. An increase in SST up to 31.4ºC in February 2009 triggered the bleaching event observed in May 2009 at the site. Acroporids showed the first sign of bleaching and paling as from January 2009 when mean SST was at 30ºC. Branching coral (P. eydouxi) and solitary coral (Fungia sp.) exhibited only 15% of their colonies showing paling by April 2009. A. cytherea, A. hyacynthus, and A. muricata showed varying bleaching conditions [Pale (P), Partially-bleached (PB) and Bleached (B)] at onset of the bleaching event whilst Acropora sp. showed only a paling of its colonies. Post-bleaching data indicated a differential recovery in visual coloration and PSII functioning among the corals. P. eydouxi and Fungia sp. showed no bleaching conditions throughout the study. P. damicornis and G. fascicularis indicated a quick coloration recovery from P to NB after the bleaching event, although their maximum quantum yield at PSII did not show significant changes in P and NB samples. A. muricata recovered faster than A. hyacynthus and A. cytherea in terms of PSII functioning. A differential recovery was observed post-bleaching event among the eight coral species, in terms of recovery of color and PSII functioning. The order of recovery was as follows: massive-like/ solitary corals > branching and semi-bulbous corals > tabular corals.
2017-01-01
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References
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: 539-550.
Baird AH, Bhagooli R, Nonaka M, Yakovleva I, Yamamoto HH, Hidaka
M, Yamasaki H. 2010. Environmental controls on the establishment
and development of algal symbiosis in corals. Proceedings of the 11th
International Coral Reef Symposium, Ft. Lauderdale, Florida, 7-11
July 2008, 108-112.
Baird AH, Marshall PA. 2002. Mortality, growth and reproduction in
scleractinian coral following bleaching on the Great Barrier Reef. Mar
Ecol Prog Ser 237: 133-141.
Baird AH, Bhagooli R, Ralph PJ, Takehashi S. 2009. Coral Bleaching: the
role of the host. Trends Ecol Evol 24: 16-20.
Baker AC, Glynn PW, Riegl B. 2008. Climate change and coral reef
bleaching: An ecological assessment of long-term impacts, recovery
trends and future outlook. Estuar Coastal Shelf Sci 80: 435-471.
Baker AC, Starger CJ, Mcclanahan TR, Glynn PW. 2004. Coral reefs:
corals’ adaptive response to climate change. Nature 430 (7001): 741.
Berkelmans R, Van Oppen MJH. 2006. The role of zooxanthellae in the
thermal tolerance of corals: a 'nugget of hope' for coral reefs in an era
of climate change. Proc R Soc London 273: 2305-2312.
Bhagooli R. 2009. Symbiont-dependent thermal bleaching susceptiblity in
two reef-building corals, Stylophora pistillata and Platygyra
ryukyuensis. Univ Mauritius Res J 15 (1): 607-626.
Bhagooli R. 2012a. The application of a bleaching index as a potential
tool for monitoring coral health. Univ Mauritius Res J 18A: 88-104.
Bhagooli R. 2012b. Light-induced production of tuberculae on exposed
coral surfaces of the coral Montipora capitata. Univ Mauritius Res J
18A: 145-165.
Bhagooli R. 2013. Inhibition of Calvin-Benson cycle suppresses the repair
of photosystem II in Symbiodinium: implications for coral bleaching.
Hydrobiologia 714 (1): 183-190.
Bhagooli R, Baird AH, Ralph PJ. 2008. Does the coral host protect its
algal symbionts from heat and light stresses. Proceedings of the 11th
International Coral Reef Symposium, Ft. Lauderdale, Florida, 7-11
July 2008, 5, 113-117.
Bhagooli R, Hidaka M. 2003. Comparison of stress susceptibility of in
hospite and isolated zooxanthellae among five coral species. J Exp
Mar Biol Ecol 291 (2): 181-197.
Bhagooli R, Hidaka M. 2006. Thermal inhibition and recovery of the
maximum quantum yield of photosystem II and the maximum
electron transport rate in zooxanthellae of a reef-building coral. J Jpn
Coral Reef Soc 8 (1): 1-11.
Bhagooli R, Yakovleva I. 2004. Differential bleaching susceptibility and
mortality patterns among four corals in response to thermal stress.
Symbiosis 37 (1-3): 121-136.
Brown B, Dunne R, Goodson M, Douglas A. 2002. Experience shapes the
susceptibility of a reef coral to bleaching. Coral Reefs 21 (2): 119-
126.
Brown BE, Suharsono. 1990. Damage and recovery of coral reefs affected
by El Nino related sea water warming in the Thousand Islands,
Indonesia, Coral Reefs 8: 163-170.
Brown BE, Dunne RP, Warner E, Ambarsari I, Fitt WK, Gibb W,
Cummings DG. 2000. Damage and recovery of Photosystem II during
a manipulative field experiment on solar bleaching in the coral
Goniastrea aspera. Mar Ecol Prog Ser 195: 117-124.
Fitt WK, Brown BE, Warner ME, Dunne RP. 2001. Coral bleaching:
Interpretation of thermal tolerance limits and thermal thresholds in
tropical corals. Coral Reefs 20: 51-65.
Fitt WK, Warner ME. 1995. Bleaching patterns of four species of
Caribbean reef corals. Biol Bull (Woods Hole) 189: 298-307.
Genty B, Briantais JM, Baker NR. 1989. The relationship between the
quantum yield of photosynthetic electron transport and quenching of
chlorophyll fluorescence. Biochimica Biophysica Acta 990: 87-92.
Grottoli AG, Rodrigues LJ, Palardy J E. 2006. Heterotrophic plasticity
and resilience in bleached corals Nature 440: 1186-1189
Iglesias-Prieto R. 1997. Temperature-dependent inactivation of
photosystem II in symbiotic dinoflagellates. Proceedings of the Eighth
International Coral Reef Symposium (Panama) 2, 1313-1318.
Iglesias-Prieto R, Matta JL, Robins WA, Trench R K. 1992.
Photosynthetic response to elevated temperature in the symbiotic
dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl
Acad Sci USA 89 10302-10305.
Jones RJ. 2008. Coral bleaching, bleaching-induced mortality, and the
adaptive significance of the bleaching response. Mar Biol 154 65-80
Jones RJ, Hoegh-Guldberg O. 2001. Diurnal changes in the
photochemical efficiency of the symbiotic dinoflagellates
(Dinophyceae) of corals: photoprotection, photoinactivation and the
relationship to coral bleaching. Plant Cell Environ 24 89-99.
Jones RJ, Yellowlees D. 1997. Regulation and control of intracellular
algae (= zooxanthellae) in hard corals. Phil Trans R Soc London 352:
457-468.
Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreider U. 1998.
Temperature-induced bleaching of corals begins with impairment of
the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21:
1219-1230.
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 R Soc B Bil Sci 276:
4139-4148.
Lesser MP. 1996. Elevated temperature and ultraviolet radiation cause
oxidative stress and inhibit photosynthesis in symbiotic
dinoflagellates. Limnol Oceanogr 41: 271-283.
Louis Y D, Kaullysing D, Gopeechund A, Mattan-Moorgawa S, Bahorun
T, Dyall S D, Bhagooli R. 2016. In hospite Symbiodinium
photophysiology and antioxidant responses in Acropora muricata on a
coast-reef scale: implications for variable bleaching patterns.
Symbiosis 68 (1-3): 61-72.
Louis YD, Bhagooli R, Kenkel CD, Baker AC, Dyall SD. 2017. Gene
expression biomarkers of heat stress in scleractinian corals: Promises
and limitations. Comp Biochem Physiol C: Toxicol Pharmacol 191:
63-77.
Loya Y, Sakai K, Yamazato K, Nakano J, Sambi H., Van Woesik R. 2001.
Cora bleaching: the winners and the losers. Ecol Lett 4: 122-131.
Mattan-Moorgawa S, Bhagooli R, Rughooputh SDDV. 2012. Thermal
stress physiology and mortality responses in scleractinian corals of
Mauritius. Proceedings of the 12th International Coral Reef
Symposium, Cairns, Australia, 9-13 July 2012. ICRS 2012, 9A,
Mc Clanahan TR. 2000. Recovery of a coral reef keystone predator,
Balistapus undulates, in East African marine parks. Biol Conserv 94:
191-198.
Mc Clanahan TR, Maina J, Moothien-Pillay R, Baker AC. 2005. Effects
of geography, taxa, water flow and temperature variation on coral
bleaching intensity in Mauritius. Mar Ecol Prog Ser 298: 131-142.
Mccowan DM, Morgan S, Pratchett MS, Baird AH. 2012. Bleaching
susceptibility and mortality among corals with differing growth
forms. Proceedings of the 12th International Coral Reef Symposium,
Cairns, Australia, 9-13 July 2012, 9A.
Muscatine L, McCloskey L R, Marian R E. 1981. Estimating the daily
contributing of carbon from zooxanthellae to coral animal respiration.
Limnol Oceanogr 36 (4): 601-610.
Nakamura T, Van Woesik R. 2001. Water flow rates and passive diffusion
partially explain differential survival of corals during the 1998
bleaching event. Mar Ecol Prog Ser 212: 301-304.
Oliver TA, Palumbi SR. 2011. Many corals host thermally resistant
symbionts in high-temperature habitat. Coral Reefs 30: 241-250.
Rodrigues LJ, Grottoli AG. 2007. Energy reserves and metabolism as
indicators of coral recovery from bleaching. Limnol Oceanogr 52:
1874-1882.
Rodrigues LJ, Grottoli AG, Lesser MP. 2008. Long-term changes in the
chlorophyll fluorescence of bleached and recovering corals from
Hawaii. J Exp Biol 211: 2502-2509.
Sampayo EM, Ridgeway T, Bongaerts P, Hoegh-Guldberg O. 2008.
Bleaching susceptibility and mortality of corals are determined by
fine-scale differences in symbiont type. Proc Natl Acad Sci USA 105
(30): 10444-10449.
Smith D J, Suggett DJ, Baker NJ. 2005. Is photoinhibition of
zooxanthellae photosynthesis the primary cause of thermal bleaching
in corals? Global Change Biol 11: 1-11.
Tchernov D, Gorbunov MY, Vargas CD, Yadav SN, Milligan AJ,
Haggblom M, Falkowski PG. 2004. Membrane lipids of symbiotic
algae are diagnostic of sensitivity to thermal bleaching in corals. Proc
Natl Acad Sci USA 101: 13531-13535.
Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW. 2006.
Multi-year, seasonal genotypic surveys of coral-algal symbioses
reveal prevalent stability or post-bleaching reversion. Mar Biol 148
711-722.
Trapido-Rosenthal H, Zielke S, Owen R, Buxton L, Boeing B, Bhagooli
R, Archer J. 2005. Increased zooxanthellae nitric oxide synthase
activity is associated with coral bleaching. Biol Bull 208: 3-6.
Van Woesik R, Sakai K, Ganase A, Loya Y. 2011. Revisiting the winners
and losers a decade after coral bleaching. Mar Ecol Prog Ser 434: 67-
76.
Visram S, Douglas AE. 2007. Resilience and acclimation to bleaching
stressors in the scleractinian coral Porites cylindrica. J Exp Mar Biol
Ecol 349 (1): 35-44.
Warner M E, Fitt W K, Schmidt G W. 1999. Damage to photosystem II in
symbiotic dinoflagellates: A determinant of coral bleaching. Proc Natl
Acad Sci USA 96: 8007-8012.
Warner ME, Fitt WK, Schmidt WG. 1996. The effects of elevated
temperature on the photosynthetic efficiency of zooxanthellae in
hospite from four different species of reef coral: a novel approach.
Plant Cell Environ 19: 291-299.
Middlebrook R. 2009. Energetics approach to predicting mortality
risk from environmental stress: a case study of coral bleaching. Funct
Ecol 23: 539-550.
Baird AH, Bhagooli R, Nonaka M, Yakovleva I, Yamamoto HH, Hidaka
M, Yamasaki H. 2010. Environmental controls on the establishment
and development of algal symbiosis in corals. Proceedings of the 11th
International Coral Reef Symposium, Ft. Lauderdale, Florida, 7-11
July 2008, 108-112.
Baird AH, Marshall PA. 2002. Mortality, growth and reproduction in
scleractinian coral following bleaching on the Great Barrier Reef. Mar
Ecol Prog Ser 237: 133-141.
Baird AH, Bhagooli R, Ralph PJ, Takehashi S. 2009. Coral Bleaching: the
role of the host. Trends Ecol Evol 24: 16-20.
Baker AC, Glynn PW, Riegl B. 2008. Climate change and coral reef
bleaching: An ecological assessment of long-term impacts, recovery
trends and future outlook. Estuar Coastal Shelf Sci 80: 435-471.
Baker AC, Starger CJ, Mcclanahan TR, Glynn PW. 2004. Coral reefs:
corals’ adaptive response to climate change. Nature 430 (7001): 741.
Berkelmans R, Van Oppen MJH. 2006. The role of zooxanthellae in the
thermal tolerance of corals: a 'nugget of hope' for coral reefs in an era
of climate change. Proc R Soc London 273: 2305-2312.
Bhagooli R. 2009. Symbiont-dependent thermal bleaching susceptiblity in
two reef-building corals, Stylophora pistillata and Platygyra
ryukyuensis. Univ Mauritius Res J 15 (1): 607-626.
Bhagooli R. 2012a. The application of a bleaching index as a potential
tool for monitoring coral health. Univ Mauritius Res J 18A: 88-104.
Bhagooli R. 2012b. Light-induced production of tuberculae on exposed
coral surfaces of the coral Montipora capitata. Univ Mauritius Res J
18A: 145-165.
Bhagooli R. 2013. Inhibition of Calvin-Benson cycle suppresses the repair
of photosystem II in Symbiodinium: implications for coral bleaching.
Hydrobiologia 714 (1): 183-190.
Bhagooli R, Baird AH, Ralph PJ. 2008. Does the coral host protect its
algal symbionts from heat and light stresses. Proceedings of the 11th
International Coral Reef Symposium, Ft. Lauderdale, Florida, 7-11
July 2008, 5, 113-117.
Bhagooli R, Hidaka M. 2003. Comparison of stress susceptibility of in
hospite and isolated zooxanthellae among five coral species. J Exp
Mar Biol Ecol 291 (2): 181-197.
Bhagooli R, Hidaka M. 2006. Thermal inhibition and recovery of the
maximum quantum yield of photosystem II and the maximum
electron transport rate in zooxanthellae of a reef-building coral. J Jpn
Coral Reef Soc 8 (1): 1-11.
Bhagooli R, Yakovleva I. 2004. Differential bleaching susceptibility and
mortality patterns among four corals in response to thermal stress.
Symbiosis 37 (1-3): 121-136.
Brown B, Dunne R, Goodson M, Douglas A. 2002. Experience shapes the
susceptibility of a reef coral to bleaching. Coral Reefs 21 (2): 119-
126.
Brown BE, Suharsono. 1990. Damage and recovery of coral reefs affected
by El Nino related sea water warming in the Thousand Islands,
Indonesia, Coral Reefs 8: 163-170.
Brown BE, Dunne RP, Warner E, Ambarsari I, Fitt WK, Gibb W,
Cummings DG. 2000. Damage and recovery of Photosystem II during
a manipulative field experiment on solar bleaching in the coral
Goniastrea aspera. Mar Ecol Prog Ser 195: 117-124.
Fitt WK, Brown BE, Warner ME, Dunne RP. 2001. Coral bleaching:
Interpretation of thermal tolerance limits and thermal thresholds in
tropical corals. Coral Reefs 20: 51-65.
Fitt WK, Warner ME. 1995. Bleaching patterns of four species of
Caribbean reef corals. Biol Bull (Woods Hole) 189: 298-307.
Genty B, Briantais JM, Baker NR. 1989. The relationship between the
quantum yield of photosynthetic electron transport and quenching of
chlorophyll fluorescence. Biochimica Biophysica Acta 990: 87-92.
Grottoli AG, Rodrigues LJ, Palardy J E. 2006. Heterotrophic plasticity
and resilience in bleached corals Nature 440: 1186-1189
Iglesias-Prieto R. 1997. Temperature-dependent inactivation of
photosystem II in symbiotic dinoflagellates. Proceedings of the Eighth
International Coral Reef Symposium (Panama) 2, 1313-1318.
Iglesias-Prieto R, Matta JL, Robins WA, Trench R K. 1992.
Photosynthetic response to elevated temperature in the symbiotic
dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl
Acad Sci USA 89 10302-10305.
Jones RJ. 2008. Coral bleaching, bleaching-induced mortality, and the
adaptive significance of the bleaching response. Mar Biol 154 65-80
Jones RJ, Hoegh-Guldberg O. 2001. Diurnal changes in the
photochemical efficiency of the symbiotic dinoflagellates
(Dinophyceae) of corals: photoprotection, photoinactivation and the
relationship to coral bleaching. Plant Cell Environ 24 89-99.
Jones RJ, Yellowlees D. 1997. Regulation and control of intracellular
algae (= zooxanthellae) in hard corals. Phil Trans R Soc London 352:
457-468.
Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreider U. 1998.
Temperature-induced bleaching of corals begins with impairment of
the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21:
1219-1230.
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 R Soc B Bil Sci 276:
4139-4148.
Lesser MP. 1996. Elevated temperature and ultraviolet radiation cause
oxidative stress and inhibit photosynthesis in symbiotic
dinoflagellates. Limnol Oceanogr 41: 271-283.
Louis Y D, Kaullysing D, Gopeechund A, Mattan-Moorgawa S, Bahorun
T, Dyall S D, Bhagooli R. 2016. In hospite Symbiodinium
photophysiology and antioxidant responses in Acropora muricata on a
coast-reef scale: implications for variable bleaching patterns.
Symbiosis 68 (1-3): 61-72.
Louis YD, Bhagooli R, Kenkel CD, Baker AC, Dyall SD. 2017. Gene
expression biomarkers of heat stress in scleractinian corals: Promises
and limitations. Comp Biochem Physiol C: Toxicol Pharmacol 191:
63-77.
Loya Y, Sakai K, Yamazato K, Nakano J, Sambi H., Van Woesik R. 2001.
Cora bleaching: the winners and the losers. Ecol Lett 4: 122-131.
Mattan-Moorgawa S, Bhagooli R, Rughooputh SDDV. 2012. Thermal
stress physiology and mortality responses in scleractinian corals of
Mauritius. Proceedings of the 12th International Coral Reef
Symposium, Cairns, Australia, 9-13 July 2012. ICRS 2012, 9A,
Mc Clanahan TR. 2000. Recovery of a coral reef keystone predator,
Balistapus undulates, in East African marine parks. Biol Conserv 94:
191-198.
Mc Clanahan TR, Maina J, Moothien-Pillay R, Baker AC. 2005. Effects
of geography, taxa, water flow and temperature variation on coral
bleaching intensity in Mauritius. Mar Ecol Prog Ser 298: 131-142.
Mccowan DM, Morgan S, Pratchett MS, Baird AH. 2012. Bleaching
susceptibility and mortality among corals with differing growth
forms. Proceedings of the 12th International Coral Reef Symposium,
Cairns, Australia, 9-13 July 2012, 9A.
Muscatine L, McCloskey L R, Marian R E. 1981. Estimating the daily
contributing of carbon from zooxanthellae to coral animal respiration.
Limnol Oceanogr 36 (4): 601-610.
Nakamura T, Van Woesik R. 2001. Water flow rates and passive diffusion
partially explain differential survival of corals during the 1998
bleaching event. Mar Ecol Prog Ser 212: 301-304.
Oliver TA, Palumbi SR. 2011. Many corals host thermally resistant
symbionts in high-temperature habitat. Coral Reefs 30: 241-250.
Rodrigues LJ, Grottoli AG. 2007. Energy reserves and metabolism as
indicators of coral recovery from bleaching. Limnol Oceanogr 52:
1874-1882.
Rodrigues LJ, Grottoli AG, Lesser MP. 2008. Long-term changes in the
chlorophyll fluorescence of bleached and recovering corals from
Hawaii. J Exp Biol 211: 2502-2509.
Sampayo EM, Ridgeway T, Bongaerts P, Hoegh-Guldberg O. 2008.
Bleaching susceptibility and mortality of corals are determined by
fine-scale differences in symbiont type. Proc Natl Acad Sci USA 105
(30): 10444-10449.
Smith D J, Suggett DJ, Baker NJ. 2005. Is photoinhibition of
zooxanthellae photosynthesis the primary cause of thermal bleaching
in corals? Global Change Biol 11: 1-11.
Tchernov D, Gorbunov MY, Vargas CD, Yadav SN, Milligan AJ,
Haggblom M, Falkowski PG. 2004. Membrane lipids of symbiotic
algae are diagnostic of sensitivity to thermal bleaching in corals. Proc
Natl Acad Sci USA 101: 13531-13535.
Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW. 2006.
Multi-year, seasonal genotypic surveys of coral-algal symbioses
reveal prevalent stability or post-bleaching reversion. Mar Biol 148
711-722.
Trapido-Rosenthal H, Zielke S, Owen R, Buxton L, Boeing B, Bhagooli
R, Archer J. 2005. Increased zooxanthellae nitric oxide synthase
activity is associated with coral bleaching. Biol Bull 208: 3-6.
Van Woesik R, Sakai K, Ganase A, Loya Y. 2011. Revisiting the winners
and losers a decade after coral bleaching. Mar Ecol Prog Ser 434: 67-
76.
Visram S, Douglas AE. 2007. Resilience and acclimation to bleaching
stressors in the scleractinian coral Porites cylindrica. J Exp Mar Biol
Ecol 349 (1): 35-44.
Warner M E, Fitt W K, Schmidt G W. 1999. Damage to photosystem II in
symbiotic dinoflagellates: A determinant of coral bleaching. Proc Natl
Acad Sci USA 96: 8007-8012.
Warner ME, Fitt WK, Schmidt WG. 1996. The effects of elevated
temperature on the photosynthetic efficiency of zooxanthellae in
hospite from four different species of reef coral: a novel approach.
Plant Cell Environ 19: 291-299.