Herbicides increase the vulnerability of corals to rising sea surface temperature

Limnology and Oceanography

Volumn 56, Issue 2, 2011, Pages 471-485

  Negri, Andrew P ^a   Flores, Florita ^a   Röthig, Till ^a   Uthicke, Sven ^a  

^a AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CLIMATE CHANGE; CONCENTRATION (COMPOSITION); CORAL; CORAL BLEACHING; ENVIRONMENTAL STRESS; NUMERICAL MODEL; PHOTOINHIBITION; PHOTOSYNTHESIS; RED ALGA; SEA SURFACE TEMPERATURE; TEMPERATURE EFFECT; VULNERABILITY; WATER QUALITY;

ACROPORA MILLEPORA; ALGAE; ANTHOZOA; NEOGONIOLITHON FOSLIEI;

EID: 79952054639     PISSN: 00243590     EISSN: None     Source Type: Journal    
DOI: 10.4319/lo.2011.56.2.0471     Document Type: Article

References (53)

1. AIMS (AUSTRALIAN INSTITUTE OF MARINE SCIENCE). 2010. Sea temperature monitoring program [Internet]. Townsville, Australia: Australian Institute of Marine Science [accessed 2010 December 14]. Available from http://www.aims.gov. au/docs/data-centre/seatemperatures.html.
2. ANTHONY, K. R. N., S. R. CONNOLLY, AND O. HOEGH-GULDBERG. 2007. Bleaching, energetics, and coral mortality risk: Effects of temperature, light, and sediment regime. Limnol. Oceanogr. 52: 716-726, doi:10.4319/lo.2007.52.2. 0716 (Pubitemid 46972307)
3. -, D. I. KLINE, G. DIAZ-PULIDO, S. DOVE, AND O. HOEGHGULDBERG. 2008. Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc. Natl. Acad. Sci. 105: 17442-17446, doi:10.1073/pnas.0804478105
4. BAIRD, A. H., AND P. A. MARSHALL. 2002. Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Mar. Ecol. Prog. Ser. 237: 133-141, doi:10.3354/meps237133
5. BELLWOOD, D. R., T. P. HUGHES, C. FOLKE, AND M. NYSTROM. 2004. Confronting the coral reef crisis. Nature 429: 827-833, doi:10.1038/nature02691 (Pubitemid 38843290)
6. BERKELMANS, R., AND M. J. H. VAN OPPEN. 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. Royal Soc. B: Biol. Sci. 273: 2305-2312, doi:10.1098/rspb.2006.3567 (Pubitemid 44387337)
7. -, AND B. L. WILLIS. 1999. Seasonal and local spatial patterns in the upper thermal limits of corals on the inshore Central Great Barrier Reef. Coral Reefs 18: 219-228, doi:10.1007/s003380050186 (Pubitemid 29478081)
8. BROWN, B. E., I. AMBARSARI, M. E. WARNER, W. K. FITT, R. P. DUNNE, S. W. GIBB, AND D. G. CUMMINGS. 1999. Diurnal changes in photochemical efficiency and xanthophyll concentrations in shallow water reef corals: Evidence for photoinhibition and photoprotection. Coral Reefs 18: 99-105, doi:10.1007/s003380050163 (Pubitemid 29365520)
9. BRUNO, J. F., AND E. R. SELIG. 2007. Regional decline of coral cover in the Indo-Pacific: Timing, extent, and subregional comparisons. PLoS ONE 2: e711, doi:10.1371/journal.pone.0000711 (Pubitemid 351330805)
10. BÜCHEL, C., AND C. WILHEM. 1993. In vivo analysis of slow chlorophyll fluorescence induction kinetics in algae: Progress, problems and perspectives. Photochem. Photobiol. 58: 137-148, doi:10.1111/j.1751-1097.1993. tb04915.x
11. CANTIN, N. E., A. P. NEGRI, AND B. L. WILLIS. 2007. Photoinhibition from chronic herbicide exposure reduces reproductive output of reef-building corals. Mar. Ecol. Prog. Ser. 344: 81-93, doi:10.3354/meps07059 (Pubitemid 47475669)
12. -, M. J. H. VAN OPPEN, B. L. WILLIS, J. C. MIEOG, AND A. P. NEGRI. 2009. Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs 28: 405-414, doi:10.1007/s00338-009-0478-8
13. CHISHOLM, J. R. M. 2003. Primary productivity of reef-building crustose coralline algae. Limnol. Oceanogr. 48: 1376-1387, doi:10.4319/lo.2003.48.4.1376 (Pubitemid 36964758)
14. DOUGLAS, A. E. 2003. Coral bleaching - how and why? Mar. Pollut. Bull. 46: 385-392, doi:10.1016/S0025-326X(03)00037-7 (Pubitemid 36434013)
15. FABRICIUS, K. E. 2005. Effects of terrestrial runoff on the ecology of corals and coral reefs: Review and synthesis. Mar. Pollut. Bull. 50: 125-146, doi:10.1016/j.marpolbul.2004.11.028 (Pubitemid 40298988)
16. FURNAS, M. J. 2003. Catchments and corals: Terrestrial runoff to the Great Barrier Reef, 1st ed. [Internet]. Townsville, Australia: Australian Institute of Marine Science and CRC Reef Research Centre [accessed 2010 December 14]. http://www.aims.gov.au/docs/research/water-quality/runoff/catchments- corals.html.
17. GBRMPA (GREAT BARRIER REEF MARINE PARK AUTHORITY). 2009. Water quality guidelines for the Great Barrier Reef Marine Park [Internet]. Townsville, Australia: Great Barrier Reef Marine Park Authority [accessed 2010 December 14]. Available from http://www.gbrmpa.gov.au/corp-site/key-issues/water-quality/ water-quality-guidelines.
18. GENTY, B., J. M. BRIANTAIS, AND N. R. BAKER. 1989. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 990: 87-92.
19. HARRINGTON, L., K. FABRICIUS, G. DE'ATH, AND A. NEGRI. 2004. Recognition and selection of settlement substrata determines post-settlement survival in corals. Ecology 85: 3428-3437, doi:10.1890/04-0298 (Pubitemid 40084790)
20. -, -, G. EAGLESHAM, AND A. NEGRI. 2005. Synergistic effects of diuron and sedimentation on photosynthesis and survival of crustose coralline algae. Mar. Pollut. Bull. 51: 415-427, doi:10.1016/j.marpolbul.2004.10.042 (Pubitemid 40341634)
21. HAYNES, D., P. J. RALPH, J. MUELLER, J. PRANGE, AND K. MICHALEK-WAGNER. 2000. The occurrence and impact of herbicides in the Great Barrier Reef Marine Park. Reef. Res. 10: 2-4.
22. HOEGH-GULDBERG, O. 1999. Climate change, coral bleaching and the future of the world's coral reefs. Mar. Freshw. Res. 50: 839-866, doi:10.1071/MF99078 (Pubitemid 30018479)
23. -, AND OTHERS. 2007. Coral reefs under rapid climate change and ocean acidification. Science 318: 1737-1742, doi:10.1126/science.1152509
24. HUGHES, T. P., AND OTHERS. 2003. Climate change, human impacts, and the resilience of coral reefs. Science 301: 929-933, doi:10.1126/science.1085046 (Pubitemid 36994796)
25. IPCC (INTERGOVERNMENTAL PANEL ON CLIMATE CHANGE). 2007. Synthesis report. Contribution of working groups I, II and III, p. 1-104. In C. W. Team, R. K. Pachauri, and A. Reisinger [EDS.], Fourth assessment report of the intergovernmental panel on climate change. IPCC.
26. JOHNSON, J., AND P. MARSHALL [EDS.] 2007. Climate change and the Great Barrier Reef: A vulnerability assessment [Internet]. Townsville, Australia: Great Barrier Reef Marine Park Authority [accessed 2010 December 14]. Available from http://www.gbrmpa.gov.au/corp-site/info-services/publications/misc-pub/ climate-change-vulnerability-assessment/climate-change-vulnerability-assessment.
27. 2 fixation mechanism in zooxanthellae. Plant Cell Environ. 21: 1219-1230, doi:10.1046/j.1365-3040.1998.00345.x (Pubitemid 29051743)
28. -, AND A. P. KERSWELL. 2003. Phytotoxicity of photosystem II (PSII) herbicides to coral. Mar. Ecol. Prog. Ser. 261: 149-159, doi:10.3354/meps261149 (Pubitemid 37425119)
29. -, J. MULLER, D. HAYNES, AND U. SCHREIBER. 2003. Effects of herbicides diuron and atrazine on corals of the Great Barrier Reef, Australia. Mar. Ecol. Prog. Ser. 251: 153-167, doi:10.3354/meps251153 (Pubitemid 36551383)
30. KLEPPEL, G. S., R. E. DODGE, AND C. J. REESE. 1989. Changes in pigmentation associated with the bleaching of stony corals. Limnol. Oceanogr. 34: 1331-1335, doi:10.4319/lo.1989.34.7.1331
31. LESSER, M. P. 1997. Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16: 187-192, doi:10.1007/ s003380050073 (Pubitemid 27362967)
32. LEWIS, S. E., J. E. BRODIE, Z. T. BAINBRIDGE, K.W. ROHDE, A. M. DAVIS, B. L. MASTERS, M. MAUGHAN, M. J. DEVLIN, J. F. MUELLER, AND B. SCHAFFELKE. 2009. Herbicides: A new threat to the Great Barrier Reef. Environ. Pollut. 157: 2470-2484, doi:10.1016/j.envpol.2009.03.006
33. MAGNUSSON, M., K. HEIMANN, AND A. P. NEGRI. 2008. Comparative effects of herbicides on photosynthesis and growth of tropical estuarine microalgae. Mar. Pollut. Bull. 56: 1545-1552, doi:10.1016/j.marpolbul.2008.05.023
34. MAXWELL, K., AND G. N. JOHNSON. 2000. Chlorophyll fluorescence - a practical guide. J. Exp. Bot. 51: 659-668, doi:10.1093/jexbot/51.345.659 (Pubitemid 30254655)
35. NAGELKERKEN, I. 2006. Relationship between anthropogenic impacts and bleaching-associated tissue mortality of corals in Curaçao (Netherlands Antilles). Int. J. Tropical Biol. 54: 31-44.
36. NEGRI, A., C. VOLLHARDT, C. HUMPHREY, A. HEYWARD, R. JONES, G. EAGLESHAM, AND K. FABRICIUS. 2005. Effects of the herbicide diuron on the early life history stages of coral. Mar. Pollut. Bull. 51: 370-383, doi:10.1016/j. marpolbul.2004.10.053 (Pubitemid 40341630)
37. NORDEMAR, I., M. NYSTRÖM, AND R. DIZON. 2003. Effects of elevated seawater temperature and nitrate enrichment on the branching coral Porites cylindrica in the absence of particulate food. Mar. Biol. 142: 669.
38. NYSTRÖM, M., I. NORDEMAR, AND M. TEDENGREN. 2001. Simultaneous and sequential stress from increased temperature and copper on the metabolism of the hermatypic coral Porites cylindrica. Mar. Biol. 138: 1225-1231, doi:10.1007/s002270100549 (Pubitemid 32620743)
39. OETTMEIER, W. 1992. Herbicides of photosystem II, p. 349-408. In J. Barber [ed.], The photosystems: Structure, function and molecular biology. Elsevier.
40. OLIVER, J. K., R. BERKELMANS, AND C. M. EAKIN. 2009. Coral bleaching in space and time, p. 21-39. In M. J. H. van Oppen and J. M. Lough [eds.], Coral bleaching. Springer.
41. OSMOND, C. B., J. M. ANDERSON, M. C. BALL, AND J. J. G. EGERTON. 1999. Compromising efficiency: The molecular ecology of light resource utilisation in terrestrial plants, p. 1-24. In C. Scholes and M. Baker [eds.], Advances in physiological plant ecology. Blackwell.
42. PANDOLFI, J. M., AND OTHERS. 2003. Global trajectories of the long-term decline of coral reef ecosystems. Science 301: 955-958, doi:10.1126/science. 1085706 (Pubitemid 36994805)
43. R DEVELOPMENT CORE TEAM. 2006. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
44. SCHUBERT, N. 2008. Phototprotective mechanisms in red algae. Ph.D. thesis. Universidad Autónoma de Baja California, Mexico.
45. SHAW, M., M. J. FURNAS, K. FABRICIUS, D. HAYNES, S. CARTER, G. EAGLESHAM, AND J. F. MUELLER. 2010. Monitoring pesticides in the Great Barrier Reef. Mar. Pollut. Bull. 60: 113-122, doi:10.1016/j.marpolbul.2009.08.026
46. SOKOLOVA, I. M., AND G. LANNIG. 2008. Interactive effects of metal pollution and temperature on metabolism in aquatic ectotherms: Implications of global climate change. Climate. Res. 37: 181-201, doi:10.3354/cr00764
47. STIMSON, J., AND R. A. KINZIE. 1991. The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen-enrichment and control conditions. J. Exp. Mar. Biol. Ecol. 153: 63-67, doi:10.1016/S0022-0981(05)80006-1
48. VAN OPPEN, M. J. H. 2004. Mode of zooxanthella transmission does not affect zooxanthella diversity in acroporid corals. Mar. Biol. 144: 1-7, doi:10.1007/s00227-003-1187-4 (Pubitemid 38106694)
49. WAKEFIELD, T. S., AND S. C. KEMPF. 2001. Development of host and symbiont-specific monoclonal antibodies and confirmation of the origin of the symbiosome membrane in a cnidarian-dinoflagellate symbiosis. Biol. Bull. 200: 127-143, doi:10.2307/1543306 (Pubitemid 32391887)
50. WARNER, M. E., W. K. FITT, AND G. W. SCHMIDT. 1999. Damage to photosystem II in symbiotic dinoflagellates: A determinant of coral bleaching. Proc. Natl. Acad. Sci. 96: 8007-8012, doi:10.1073/pnas.96.14.8007 (Pubitemid 29328398)
51. WEBSTER, N. S., R. SOO, R. COBB, AND A. P. NEGRI. In press. Elevated seawater temperature causes a microbial shift on crustose coralline algae with implications for the recruitment of coral larvae. ISME Journal, doi:10.1038/ismej.2010.152
52. WILKINSON, C. 2008. Status of coral reefs of the world: 2008, 5th Global report [Internet]. Townsville, Australia: Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre [accessed 2010 December 14]. Available from http://www.reefbase.org/resource-center/publication/main.aspx?refid= 27173&referrer=GCRMN.
53. WOOLDRIDGE, S. A. 2009. Water quality and coral bleaching thresholds: Formalising the linkage for the inshore reefs of the Great Barrier Reef, Australia. Mar. Pollut. Bull. 58: 745-751, doi:10.1016/j.marpolbul.2008.12.013