Abstract
Tolerance to hyposalinity of the scleractinian coral S. radians was examined in a mesocosm study. Colonies of S. radians were collected from five basins in Florida Bay, USA, which occur along a northeast-to-southwest salinity gradient. Salinity treatments were based on historical salinity records for these basins. Photophysiology of the endosymbiont Symbiodinium spp. (maximum quantum yield; Fv/Fm) was measured as an indicator of holobiont stress to hyposalinity. Colonies from each basin were assigned four salinity treatments [The Practical Salinity Scale (PSS) was used to determine salinity. Units are not assigned to salinity values because it is a ratio and has no unit as defined by UNESCO (UNESCO Technical papers no. 45, IAPSO Pub. Sci. No. 32, Paris, France, 1985)] (30, 20, 15, and 10) and salinities were reduced 2 per day from ambient (30) to simulate a natural salinity decrease. Colonies treated with salinities of 20 and 15 showed no decrease in Fv/Fm versus controls (i.e. 30), up to 5 days after reaching their target salinity. This indicates a greater ability to withstand reduced salinity for relatively extended periods of time in S. radians compared to other reef species. Within 1 day after salinity of 10 was reached, there was a significant reduction in Fv/Fm, indicating a critical threshold for hyposaline tolerance. At the lowest treatment salinity (10), Fv/Fm for the more estuarine, northeast-basin colonies were significantly higher than the most marine southwest-basin colonies (Twin Key Basin). Our results suggest that historical salinity ranges within basins determine coral population salinity tolerances.
Similar content being viewed by others
References
Anthony KR, Conolly SR, Willis BL (2002) Comparative analysis of energy allocation to tissue and skeletal growth in corals. Limnol Oceanogr 47(5):1417–1429
Army US Corps of Engineers and South Florida Water Management District (2000) Master Program Management Plan, vol I. http://www.evergladesplan.org/pm/program_docs/mpmp.aspx
Becker G, Norman J, Moholl-Siebett M (1990) Two sites of heat-induced damage to photosystem II. In: Baltscheffsky M (ed) Current research in photosynthesis, vol IV. Kluwer, Dordrecht, pp 705–708
Ben-Amotz A (1973) The role of glycerol in the osmotic regulation of the halophilic alga Dunaliella parva. J Phycol 51:875–878
Blank RJ, Trench RK (1985) Speciation and symbiotic dinoflagellates. Science 229:656–658. doi:https://doi.org/10.1126/science.229.4714.656
Carpenter LW, Patterson MR (2007) Water flow influences the distribution of photosynthetic efficiency within colonies of the scleractinian coral Montastrea annularis (Ellis and Solander, 1786); implications for coral bleaching. J Exp Mar Biol 351:10–26. doi:https://doi.org/10.1016/j.jembe.2007.05.022
Chartrand KM, Durako MJ (2009) Distribution and photobiology of Siderastrea radians and Thalassia testudinum in Florida Bay, FL USA. Bull Mar Sci 84(2):153–166
Chitlaru E, Pick U (1991) Regulation of glycerol synthesis in response to osmotic changes in Dunaliella. Plant Physiol 96:50–60. doi:https://doi.org/10.1104/pp.96.1.50
Coles SL, Jokiel PL (1992) Effects of salinity on corals. In: Connell DW, Hawker DW (eds) Pollution in tropical aquatic systems. CRC Press, Boca Raton, pp 147–166
Durako MJ, Chartrand KM (2009) Changes in spectral reflectance in response to salinity variation in Siderastrea radians from Florida Bay, Florida USA. In: Proceedings of the 11th international coral reef symposium, Ft. Lauderdale, FL, 7–11 July 2008 (in press)
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. doi:https://doi.org/10.1007/s003380100146
Gates RD, Edmunds PJ (1999) The physiological mechanisms of acclimatization in tropical reef corals. Am Zool 39:30–43
Gates RD, Hoegh-Guldberg O, McFall-Ngai MJ, Bil KY, Muscatine L (1995) Free amino acids exhibit anthozoan host factor activity: they induce the release of photosynthate from freshly isolated symbiotic dinoflagellates in vitro. Proc Natl Acad Sci USA 92:7430–7434. doi:https://doi.org/10.1073/pnas.92.16.7430
Gross E, Dilley RA, San Pietro A (1969) Control of electron flow in chloroplasts by cations. Arch Biochem Biophys 134:450–462. doi:https://doi.org/10.1016/0003-9861(69)90305-1
Guinotte JM, Buddemeier RW, Kleypas JA (2003) Future coral reef habitat marginality: temporal and spatial effects of climate change in the Pacific basin. Coral Reefs 22:551–558. doi:https://doi.org/10.1007/s00338-003-0331-4
Hackney JW, Durako MJ (2004) Size-frequency patterns in morphometric characteristics of the seagrass Thalassia testudinum reflect environmental variability. Ecol Indic 4:55–71. doi:https://doi.org/10.1016/j.ecolind.2003.12.001
Hill R, Schreiber U, Gademann R, Larkum AWD, Kuhl M, Ralph PJ (2004) Spatial heterogeneity of photosynthesis and the effect of temperature induced bleaching conditions in three species of corals. Mar Biol (Berl) 144:633–640. doi:https://doi.org/10.1007/s00227-003-1226-1
Hill R, Frankart C, Ralph PJ (2005) Impact of bleaching conditions on the components of non-photochemical quenching in the zooxanthellae of a coral. J Exp Mar Biol Ecol 22(1):83–92. doi:https://doi.org/10.1016/j.jembe.2005.02.011
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the word’s coral reefs. Mar Freshw Res 50:839–866. doi:https://doi.org/10.1071/MF99078
Hoegh-Guldberg O, Jones RJ (1999) Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Mar Ecol Prog Ser 183:73–86. doi:https://doi.org/10.3354/meps183073
Iglesias-Prieto R, Matta JL, Robins WA, Trench RK (1992) Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl Acad Sci USA 89:10302–10305. doi:https://doi.org/10.1073/pnas.89.21.10302
Iglesias-Prieto R, Beltran VH, LaJeunesse TC, Reyes-Bonilla H, Thome PE (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the Eastern Pacific. Proc R Soc Lond Ser B Biol Sci 271:1757–1763. doi:https://doi.org/10.1098/rspb.2004.2757
Jahnke LS, White AL (2003) Long-term hyposaline and hypersaline stresses produce distinct antioxidant responses in the marine alga Dunaliella tertiolecta. J Plant Physiol 160:1193–1202. doi:https://doi.org/10.1078/0176-1617-01068
Jones RJ, Hoegh-Guldberg O (1999) Effects of cyanide on coral photosynthesis: implications for identifying the cause of coral bleaching and for assessing the environmental effects of cyanide fishing. Mar Ecol Prog Ser 177:83–91. doi:https://doi.org/10.3354/meps177083
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. doi:https://doi.org/10.1046/j.1365-3040.2001.00648.x
Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U (1998) Temperature induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21:1219–1230. doi:https://doi.org/10.1046/j.1365-3040.1998.00345.x
Jones RJ, Kildea T, Hoegh-Guldberg O (1999) PAM chlorophyll fluorometry: a new in situ technique for stress assessment in scleractinian corals, used to examine the effect of cyanide from cyanide fishing. Mar Pollut Bull 38:864–874. doi:https://doi.org/10.1016/S0025-326X(98)90160-6
Jones RJ, Ward S, Amri AY, Hoegh-Guldberg O (2000) Changes in quantum efficiency of Photosystem II of symbiotic dinoflagellates of corals alter heat stress, and of bleached corals sampled alter the 1998 Great Barrier Ref. mass bleaching event. Mar Freshw Res 51:63–71. doi:https://doi.org/10.1071/MF99100
Kahn AE, Durako MJ (2005) The effect of salinity and ammonium on seed germination in Ruppia maritima from Florida Bay. Bull Mar Sci 77:453–458
Kahn AE, Durako MJ (2006) Thalassia testudinum seedling responses to changes in and nitrogen. J Exp Mar Biol Ecol 335:1–12. doi:https://doi.org/10.1016/j.jembe.2006.02.011
Kerswell AP, Jones RJ (2003) Effects of hypo-osmosis on the coral Stylophora pistillata: nature and cause of ‘low-salinity bleaching’. Mar Ecol Prog Ser 253:145–154. doi:https://doi.org/10.3354/meps253145
LaJeunnesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a ‘species’ level marker. J Phycol 37(5):866–880. doi:https://doi.org/10.1046/j.1529-8817.2001.01031.x
Lewis JB (1989) Spherical growth in the Caribbean coral Siderastrea radians (Pallas) and its survival in disturbed habitats. Coral Reefs 7:161–167. doi:https://doi.org/10.1007/BF00301594
Light S, Dineen W (1994) Water control in the Everglades: a historical perspective. In: Ogden SM, Ogden JC (eds) Everglades the ecosystem and its restoration. St Lucie Press, Delray Beach
Lirman D (2002) Back from the dead: the resilience of Siderastrea radians to severe stress. Coral Reefs 21:291–292
Lirman D, Orlando B, Macia S, Manzello D, Kaufman L, Biber P, Jones T (2003) Coral communities of Biscayne Bay, Florida and adjacent offshore areas: diversity, abundance, distribution, and environmental correlates. Aq Conserv Mar Fres Eco 13:121–135. doi:https://doi.org/10.1002/aqc.552
Loya Y, Saka K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131. doi:https://doi.org/10.1046/j.1461-0248.2001.00203.x
Manzello D, Lirman D (2003) The photosynthetic resilience of Porites furcata to salinity disturbance. Coral Reefs 22:537–540. doi:https://doi.org/10.1007/s00338-003-0327-0
Marcus J, Thornhaug A (1981) Pacific versus Atlantic responses of the subtropical hermatypic coral Porites spp. to temperature and salinity effects. In: Proceedings of the 4th international coral reef symposium, Quezon City, vol 2, pp 15–20
Mayfield AB, Gates RD (2007) Osmoregulation in anthozoan-dinoflagellate symbiosis. Comp Biochem Phys Part A 147:1–10. doi:https://doi.org/10.1016/j.cbpa.2006.12.042
Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinsky Z (ed) Ecosystems of the world: coral reefs. Elsevier, Amsterdam, pp 75–87
Muthiga MA, Szmant AM (1987) The effects of salinity stress on the rates of aerobic and photosynthesis in the hermatypic coral Siderastrea siderea. Biol Bull 173:539–551. doi:https://doi.org/10.2307/1541699
Nuttle WK, Fourqurean JW, Cosby BJ, Zieman JC, Robblee MB (2000) The influence of net freshwater supply on salinity in Florida Bay. Water Resour Res 36(7):1805–1822. doi:https://doi.org/10.1029/1999WR900352
Philipp E, Fabricius K (2003) Photophysiological stress in scleractinian corals in response to short-term sedimentation. J Exp Mar Biol Ecol 287:57–78
Ralph PJ, Larkum AWD, Kuhl M (2005) Temporal patterns in effective quantum yield of individual zooxanthellae expelled during bleaching. J Exp Mar Biol Ecol 316:17–28. doi:https://doi.org/10.1016/j.jembe.2004.10.003
Rinkevich B (1989) The contribution of photosynthetic products to coral reproduction. Mar Biol (Berl) 101(2):259–263. doi:https://doi.org/10.1007/BF00391465
Rodríguez-Román AR, Hernández-Pech X, Thome PE, Enríquez S, Iglesias-Prieto R (2006) Photosynthesis and light utilization in the Caribbean coral Montastraea faveolata recovering from a bleaching event. Limnol Oceanogr 51(6):2702–2710
Rowan R (1998) Diversity and ecology of zooxanthellae on coral reefs. J Phycol 344:7–17
Rudnick D (2006) Report on algae blooms in Eastern Florida Bay and Southern Biscayne Bay. South Florida Water Management District, Florida
Sampayo EM, Franceschinis L, Hoegh-Guldberg O, Dove S (2007) Niche partitioning of closely related symbiotic dinoflagellates. Mol Ecol 16:3721–3733. doi:https://doi.org/10.1111/j.1365-294X.2007.03403.x
Saxby T, Dennison WC, Hoegh-Guldberg O (2003) Photosynthetic responses of the coral Montipora digitata to cold temperature stress. Mar Ecol Prog Ser 248:85–97. doi:https://doi.org/10.3354/meps248085
Schick HM (1991) Functional biology of sea anemones. Chapman and Hall, London
Schomer NS, Drew RD (1982) An ecological characterization of the lower Everglades, Florida Bay, and the Florida Keys: U.S. Fish and Wildlife Service. Off Biol Serv FWS OBS-82(58)
Smith NP (2002) Florida bay circulation studies. Recent Res Dev Geophys 4:93–104
Trench RK (1979) The cell biology of plant animal symbioses. Annu Rev Plant Physiol 30:485–531. doi:https://doi.org/10.1146/annurev.pp.30.060179.002413
Trench RK (1993) Microalgal-invertebrate symbiosis: a review. Endo Cell Res 9:135–175
UNESCO (1985) The international system of units (SI) in oceanography. UNESCO technical papers no. 45, IAPSO Pub. Sci. No. 32, Paris, France
van Oppen MJH, Mahiny AJ, Done TJ (2005) Geographic distribution of zooxanthellae types in three coral species on the Great Barrier Reef sampled after the 2002 bleaching event. Coral Reefs 24:482–487
Veron JEN (2000) Corals of the world. Australian Institute of Marine Science, Townsville
Warner ME, Fitt WK, Schmidt GW (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. doi:https://doi.org/10.1111/j.1365-3040.1996.tb00251.x
Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci USA 96:8007–8012. doi:https://doi.org/10.1073/pnas.96.14.8007
Warner ME, Chilcoat GC, McFarland FK, Fitt WK (2002) Seasonal fluctuations in the photosynthetic capacity of photosystem II in symbiotic dinoflagellates in the Caribbean reef-building coral Montastrea. Mar Biol (Berl) 141:31–38. doi:https://doi.org/10.1007/s00227-002-0807-8
Xia J, Li Y, Zou D (2004) Effects of salinity stress on PSII in Ulva lactuca as probed by chlorophyll fluorescence measurements. Aquat Bot 80:129–137. doi:https://doi.org/10.1016/j.aquabot.2004.07.006
Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero CN (1982) Living with water stress: evolution of osmolyte systems. Science 217:1214–1222. doi:https://doi.org/10.1126/science.7112124
Acknowledgments
This research was funded by a grant from the Florida Fish and Wildlife Conservation Commission (Grant No. 56980) supported by a cooperative agreement with the South Florida Water Management District (SFWMD #4600001348). Additional data was provided by the SERC-FIU Water Quality Monitoring Network which is supported by SFWMD/SERC Cooperative Agreement #C-15397 as well as EPA Agreement #X994621-94-0. All corals were collected under the Everglades National Park research permit No. EVER-2006-SCI-0033. The authors would also like to thank Fay Belshe and Brooke Landry from UNCW and Manuel Merello, Donna Berns, Jennifer Kunzelman, and Dr. Margaret Hall from the Florida Fish and Wildlife Commission for field and logistical support.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Kühl.
Rights and permissions
About this article
Cite this article
Chartrand, K.M., Durako, M.J. & Blum, J.E. Effect of hyposalinity on the photophysiology of Siderastrea radians . Mar Biol 156, 1691–1702 (2009). https://doi.org/10.1007/s00227-009-1204-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-009-1204-3