Abstract
Bleaching (visible loss of symbiont color) in populations of the diatom-bearing foraminifer Amphistegina has been recorded from reefs worldwide since 1991. Field studies and previous laboratory experiments have strongly implicated solar radiation as a factor in bleaching stress. The influence of spectral quality and quantity of photosynthetically active radiation (PAR) and ultraviolet radiation (UV) on growth rates and bleaching in Amphistegina gibbosa was investigated in the laboratory using fluorescent sources of PAR (‘blue’ with a spectral peak at 450 nm and ‘white’ with a 600-nm spectral peak) and biologically effective ultraviolet radiation [UVB (280–320 nm)]. Growth rate, as indicated by increase in maximum shell diameter, saturated at a PAR of 6–8 μmol photon m−2 s−1, increased in ‘blue’ light, and was not influenced by UVB≤0.0162 W m−2. Frequency of bleaching increased with increasing PAR photon flux density and with exposure to shorter wavelengths, with or without an increase in total energy. Growth was significantly inhibited by UVB at 0.105 W m−2. Specimens in treatments exposed to UVB to PAR ratios >0.003 became dark in color, rather than bleaching, which previous cytological studies indicate is a photo-protective response. Implications of these experiments are that environmental factors that affect either the spectral quality or quantity of solar radiation can influence bleaching in Amphistegina.
Similar content being viewed by others
Notes
Sensors used by Gleason and Wellington (1995) measured UVB between 300 and 320 nm while our experimental doses were calculated from 290 to 320 nm. However, note from Fig. 2 that our artificial UVB source emitted very little irradiance between 290 and 320 nm; on average only 4% of the maximum dose rate was emitted in this range making the laboratory magnitudes comparable to measurements in their field study.
References
Baker AC (2000) Reef corals bleach to survive change. Nature 411:765–766
Conover WJ (1980) Practical nonparametric statistics, 2nd edn. John Wiley, New York, pp 229–233
Dunlap WC, Shick JM (1998) Ultraviolet radiation-absorbing micosporine-like amino acids in coral reef organisms: a biochemical and environmental perspective. J Phycol 34:418–430
Fitt WK, Warner ME (1995) Bleaching patterns of four species of Caribbean reef corals. Biol Bull 189:298–307
Gleason DF, Wellington GM (1995) Variation in UVB sensitivity of planula larvae of the coral Agaricia agaricites along a depth gradient. Mar Biol 123:63–703
Hallock P (1999) Symbiont-bearing Foraminifera. In: Sen Gupta BK (ed) Modern Foraminifera. Kluwer, Great Britain, pp 123–139
Hallock P, Talge HK (1994) A predatory foraminifer, Floresina amphiphaga n. sp., from the Florida Keys. J Foramin Res 24:210–213
Hallock P, Forward LB, Hansen HJ (1986) Influence of environment on the test shape of Amphistegina. J Foramin Res 16:224–231
Hallock P, Talge HK, Smith K, Cockey EM (1993) Bleaching in a reef-dwelling foraminifer, Amphistegina gibbosa. Proceedings of the 7th International Coral Reef Symposium, Guam, vol 1, pp 44–49
Hallock P, Talge HK, Cockey EM, Muller RG (1995) A new disease in reef-dwelling foraminifera: implications for coastal sedimentation. J Foramin Res 25:280–286
Hohenegger J, Yordanova E, Nakano Y, Tatzreiter F (1999) Habitats of larger foraminifera on the upper reef slope of Sesoko Island, Okinawa, Japan. Mar Micropaleontol 36:109–16
Iturriaga R, Mitchell BG, Kiefer DA (1988) Microphotometric analysis of individual particle absorption spectra. Limnol Oceanogr 33:128–135
Kirk JTO (1994) Light and photosynthesis in aquatic ecosystems. Cambridge University Press, Cambridge
Kuile BH ter, Erez J (1991) Carbon budgets for two species of benthonic symbiont-bearing foraminifera. Biological Bulletin 180:489–495
Kuile BH ter, Erez J, Lee JJ (1987) The role of feeding in the metabolism of larger symbiont bearing foraminifera. Symbiosis 4:335–350
Langer MR, Hottinger L (2000) Biogeography of selected “larger” foraminifera. Micropaleontology 46[Suppl 1]:105–126
Lee JJ, McEnery ME, Koestler RJ, Lee MJ, Reidy J, Shilo M (1983) Experimental studies of symbiont persistence in Amphistegina lessonii, a diatom-bearing species of larger foraminifera from the Red Sea. Endocytobiology 2:487–514
Lee JJ, Morales J, Symons A, Hallock P (1995) Diatom symbionts in larger foraminifera from Caribbean hosts. Mar Micropaleontol 26:99–105
Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192
Lesser MP (2000) Depth-dependent photoacclimatization to solar ultraviolet radiation in the Caribbean coral Montastraea faveolata. Mar Ecol Prog Ser 192:137–151
Lesser MP, Shick JM (1989) Photoadaptation and defenses against oxygen toxicity in zooxanthellae from natural populations of symbiotic cnidarians. J Exp Mar Biol Ecol 134:129–141
Muller PH (1978) 14Carbon fixation and symbiont loss in a foraminiferal-algal symbiont system. J Foramin Res 8:35–41
Madronich S (1992) Implications of recent total atmospheric ozone measurements for biologically active ultraviolet radiation reaching the Earth’s surface. Geophys Res Lett 19:37–40
Neale PJ (1987) Algal photoinhibition and photosynthesis in the aquatic environment. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier, Amsterdam
Randel WJ, Fei W, Russell JM III, Waters JW, Froidevaux L (1995) Ozone and temperature changes in the stratosphere following the eruption of Mt. Pinatubo. J Geophys Res 100:16753–16764
Richardson K, Beardall J, Raven JA (1983) Adaptation of unicellular algae to irradiance: an analysis of strategies. New Phytol 93:157–191
Rowan R (1998) Diversity and ecology of zooxanthellae on coral reefs. J Phycol 34:407–417
Shick JM, Lesser MP, Jokiel PL (1996) Effects of ultraviolet radiation on corals and other coral reef organisms. Glob Change Biol 2:527–545
StatSoft Inc (2001) STATISTICA for Windows.Computer program manual. StatSoft, Tulsa, Okla., USA. http://www.statsoft.com. Cited 2 March 2003
Talge HK (2002) Cytology of symbiont loss (bleaching) in Amphistegina gibbosa (Class Foraminifera). PhD dissertation, University of South Florida, Tampa, Florida
Talge HK, Hallock P (1995) Cytological examination of symbiont loss in a benthic foraminifera, Amphistegina gibbosa. Mar Micropaleontol 26:107–113
Talge HK, Hallock P (2003) Ultrastructural responses to bleaching in Amphistegina gibbosa (Foraminifera). J Eucaryot Microbiol 50:324–333
Talge HK, Williams DE, Hallock P, Harney JN (1997) Symbiont loss in reef foraminifera: consequences for affected populations. Proceedings of the 8th International Coral Reef Symposium, Panama, vol 1, pp 589–594
Toler SK, Hallock P (1998) Shell malformation in stressed Amphistegina populations: relation to biomineralization and paleoenvironmental potential. Mar Micropaleontol 34:107–115
Travis JL, Bowser SS (1991) The motility of Foraminifera. In: Lee JJ, Anderson OR (eds) Biology of Foraminifera. Academic , New York, p 91–155
Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. P Natl Acad Sci USA 96:8007–8012
Williams DE, Hallock P, Talge HK, Harney JN, McRae G (1997) Responses of Amphistegina gibbosa populations in the Florida Keys (U.S.A.) to a multi-year stress event (1991–1996). J Foramin Res 27:264–269
Zar JH (1984) Biostatistical analysis. Prentice Hall, Englewood Cliffs, N.J.
Zmiri A, Kahan D, Hochstein S, Reiss Z (1974) Phototaxis and thermotaxis in some species of Amphistegina (Foraminifera). J Protozool 21:133–138
Acknowledgements
This work was funded by the National Science Foundation (NSF OCE-9203278), the Office of Naval Research (ONR-N00014-94-1-0871) and the U.S. Environmental Protection Agency (USEPA-ORD STAR GAD-R825869). Specimens for experiments were collected during field work funded by NOAA-NURC (subcontracts nos. 9703.66 and 9922). We thank Dr. Gerald Wellington of the University of Houston for providing access to selected radiometer data. All experiments described comply with the laws of the United States of America.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by P.W. Sammarco, Chauvin
Rights and permissions
About this article
Cite this article
Williams, D.E., Hallock, P. Bleaching in Amphistegina gibbosa d’Orbigny (Class Foraminifera): observations from laboratory experiments using visible and ultraviolet light. Marine Biology 145, 641–649 (2004). https://doi.org/10.1007/s00227-004-1351-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-004-1351-5