Copper enrichment reduces thermal tolerance of the highly resistant Red Sea coral Stylophora pistillata

Abstract

Corals in the Gulf of Aqaba (GoA) in the northern Red Sea show high thermal tolerance. The GoA has therefore been suggested as a coral reef refuge from climate change. However, as a narrow body of water with high residence time and a rapidly growing population, the GoA is prone to anthropogenic stressors, heavy metal pollution being one such stressor. In the present study, the branching coral Stylophora pistillata, extensively studied for its high resistance to elevated seawater temperature in the GoA, was exposed to combinations of thermal treatments (ambient (21–23 °C), + 4 °C and + 8 °C above ambient) and ecologically relevant copper (Cu) concentrations (ambient and + 1 µg L−1 above ambient concentration). Significant interactions were found between elevated temperature and Cu enrichment effects on coral physiology, mainly affecting processes associated with photosynthesis. Contrasting responses were recorded at 72 h and 2 weeks from start of the exposure to Cu enrichment. Cu enrichment caused a decrease in Fv/Fm, maximum rETR, and net photosynthesis in ambient temperature after Cu exposure of 72 h, while at the second sampling point only (2 weeks), a decrease was also recorded at + 4 and + 8 °C. Superoxide dismutase activity was higher in Cu-enriched conditions, suggesting that corals were responding to oxidative stress. Thus, a higher input of Cu in the GoA may be energetically costly and might result in decreased resistance of corals to thermal stress under warming scenarios.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Abuhilal AH, Badran MM (1990) Effect of Pollution Sources on Metal Concentration in Sediment Cores From the Gulf of Aqaba (Red-Sea). Mar Pollut Bull 21:190–197

    Article  CAS  Google Scholar 

  2. Ali AAM, Hamed MA, Abd El-Azim H (2011) Heavy metals distribution in the coral reef ecosystems of the Northern Red Sea. Helgoland Mar Res 65:67–80

    Article  Google Scholar 

  3. Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci 105:17442–17446

    Article  PubMed  Google Scholar 

  4. Bellworthy J, Fine M (2017) Beyond peak summer temperatures, branching corals in the Gulf of Aqaba are resilient to thermal stress but sensitive to high light. Coral Reefs 36:1071–1082

    Article  Google Scholar 

  5. Bellworthy J, Fine M (2018) The Red Sea Simulator: A high-precision climate change mesocosm with automated monitoring for the long-term study of coral reef organisms. Limnol Oceanogr Methods 00-00

  6. Bielmyer GK, Grosell M, Bhagooli R, Baker AC, Langdon C, Gillette P, Capo TR (2010) Differential effects of copper on three species of scleractinian corals and their algal symbionts (Symbiodinium spp.). Aquat Toxicol 97:125–133

    Article  CAS  PubMed  Google Scholar 

  7. Biscéré T, Ferrier-Pagès C, Gilbert A, Pichler T, Houlbrèque F (2018) Evidence for mitigation of coral bleaching by manganese. Sci Rep 8:1–10

    Article  CAS  Google Scholar 

  8. Biscéré T, Rodolfo-Metalpa R, Lorrain A, Chauvaud L, Thébault J, Clavier J, Houlbrèque F (2015) Responses of two scleractinian corals to cobalt pollution and ocean acidification. PLoS One 10:1–18

    Article  CAS  Google Scholar 

  9. Biscéré T, Lorrain A, Rodolfo-Metalpa R, Gilbert A, Wright A, Devissi C, Peignon C, Farman R, Duvieilbourg E, Payri C, Houlbrèque F (2017) Nickel and ocean warming affect scleractinian coral growth. Mar Pollut Bull 120:250–258

    Article  CAS  PubMed  Google Scholar 

  10. Bradford MM (1976) A Rapid and Sensitive Method for the Quantitation Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Anal Biochem 254:248–254

    Article  Google Scholar 

  11. Caldwell PR (2016) Comparative Study of Biomarker and Fluorescence from Cultured Corals and Coral Larvae Impacted by Bunker C, Diesel Fuel, Copper and Increased Temperature. ProQuest Diss Theses Glob Retrieved 10118519

  12. Carilli JE, Norris RD, Black BA, Walsh SM, McField M (2009) Local stressors reduce coral resilience to bleaching. PLoS One 4:e6324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Chase Z, Paytan A, Beck A, Biller D, Bruland K, Measures C, Sañudo-Wilhelmy S (2011) Evaluating the impact of atmospheric deposition on dissolved trace-metals in the Gulf of Aqaba, Red Sea. Mar Chem 126:256–268

    Article  CAS  Google Scholar 

  14. Courtial L, Roberty S, Shick JM, Houlbrèque F, Ferrier-Pagès C (2017) Interactive effects of ultraviolet radiation and thermal stress on two reef-building corals. Limnol Oceanogr 62:1000–1013

    Article  Google Scholar 

  15. Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: Review and synthesis. Mar Pollut Bull 50:125–146

    Article  CAS  PubMed  Google Scholar 

  16. Ferrier-Pagès C, Sauzéat L, Balter V (2018) Coral bleaching is linked to the capacity of the animal host to supply essential metals to the symbionts. Glob Chang Biol 24:3145–3157

    Article  PubMed  Google Scholar 

  17. Ferrier-Pagès C, Schoelzle V, Jaubert J, Muscatine L, Hoegh-Guldberg O (2001) Response of a scleractinian coral, Stylophora pistillata, to iron and nitrate enrichment. J Exp Mar Biol Ecol 259:249–261

    Article  PubMed  Google Scholar 

  18. Ferrier-Pagès C, Houlbrèque F, Wyse E, Richard C, Allemand D, Boisson F (2005) Bioaccumulation of zinc in the scleractinian coral Stylophora pistillata. Coral Reefs 24:636–645

    Article  Google Scholar 

  19. Fine M, Gildor H, Genin A (2013) A coral reef refuge in the Red Sea. Glob Chang Biol 19:3640–3647

    Article  PubMed  Google Scholar 

  20. Fonseca J da S, Marangoni LF de B, Marques JA, Bianchini A (2017) Effects of increasing temperature alone and combined with copper exposure on biochemical and physiological parameters in the zooxanthellate scleractinian coral Mussismilia harttii. Aquat Toxicol 190:121–132

  21. Gajić G, Stamenković M, Pavlović P (2018) Plant Photosynthetic Response to Metal(loid) Stress. Environ Photosynth A Futur Prospect 145–209

  22. Guzmán HM, Jiménez CE (1992) Contamination of coral reefs by heavy metals along the Caribbean coast of Central America (Costa Rica and Panama). Mar Pollut Bull 24:554–561

    Article  Google Scholar 

  23. Hall ER, Muller EM, Goulet T, Bellworthy J, Ritchie KB, Fine M (2018) Eutrophication may compromise the resilience of the Red Sea coral Stylophora pistillata to global change. Mar pollut Bull 131:701–711

    Article  CAS  PubMed  Google Scholar 

  24. Harland AD, Brown BE (1989) Metal tolerance in the scleractinian coral Porites lutea. Mar Pollut Bull 20:352–357

    Article  Google Scholar 

  25. Haywood MDE, Dennis D, Thomson DP, Pillans RD (2016) Mine waste disposal leads to lower coral cover, reduced species richness and a predominance of simple coral growth forms on a fringing coral reef in Papua New Guinea. Mar Environ Res 115:36–48

    Article  CAS  PubMed  Google Scholar 

  26. Holmes G (2008) Estimating three-dimensional surface areas on coral reefs. J Exp Mar Biol Ecol 365:67–73

    Article  Google Scholar 

  27. Horwitz R, Borell EM, Fine M, Shaked Y (2014) Trace element profiles of the sea anemone Anemonia viridis living nearby a natural CO2 vent. PeerJ 2:e538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Hughes TP, Kerry JT, Simpson T (2018) Large-scale bleaching of corals on the Great Barrier. Reef Ecology 99:501

    Article  CAS  PubMed  Google Scholar 

  29. Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanzen 167:191–194

    Article  CAS  Google Scholar 

  30. Jones RJ (2004) Testing the “photoinhibition” model of coral bleaching using chemical inhibitors. Mar Ecol Prog Ser 284:133–145

    Article  CAS  Google Scholar 

  31. Knowlton N, Jackson JBC (2008) Shifting baselines, local impacts, and global change on coral reefs. PLoS Biol 6:0215–0220

    Article  CAS  Google Scholar 

  32. Krueger T, Horwitz N, Bodin J, Giovani M-E, Escrig S, Meibom A, Fine M (2017) Common reef-building coral in the Northern Red Sea resistant to elevated temperature and acidification. R Soc Open Sci 4:170038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192

    Article  Google Scholar 

  34. Lough JM, Anderson KD, Hughes TP (2018) Increasing thermal stress for tropical coral reefs: 1871–2017. Sci Rep 8:6079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Loya Y, Lubinevsky H, Rosenfeld M, Kramarsky-Winter E (2004) Nutrient enrichment caused by in situ fish farms at Eilat, Red Sea is detrimental to coral reproduction. Mar Pollut Bull 49:344–353

    Article  CAS  PubMed  Google Scholar 

  36. Marangoni LFB, Marques JA, Duarte GAS, Pereira CM, Calderon EN, Castro CB e., Bianchini A (2017) Copper effects on biomarkers associated with photosynthesis, oxidative status and calcification in the Brazilian coral Mussismilia harttii (Scleractinia, Mussidae). Mar Environ Res 130:248–257

  37. Marangoni LFB, Pinto MM de AN, Marques JA, Bianchini A (2019) Copper exposure and seawater acidification interaction: Antagonistic effects on biomarkers in the zooxanthellate scleractinian coral Mussismilia harttii. Aquat Toxicol 206:123–133

  38. Metian M, Hédouin L, Ferrier-Pagès C, Teyssié JL, Oberhansli F, Buschiazzo E, Warnau M (2015) Metal bioconcentration in the scleractinian coral Stylophora pistillata: investigating the role of different components of the holobiont using radiotracers. Environ Monit Assess 187:178

    Article  CAS  PubMed  Google Scholar 

  39. Miller AF (2012) Superoxide dismutases: Ancient enzymes and new insights. FEBS Lett 586:585–595

    Article  CAS  PubMed  Google Scholar 

  40. Millero F, Woosley R, DiTrolio B, Waters J (2009) Effect of Ocean Acidification on the Speciation of Metals in Seawater. Oceanography 22:72–85

    Article  Google Scholar 

  41. Mitchelmore CL, Verde EA, Weis VM (2007) Uptake and partitioning of copper and cadmium in the coral Pocillopora damicornis. Aquat Toxicol 85:48–56

    Article  CAS  PubMed  Google Scholar 

  42. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  Google Scholar 

  43. Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: A guide to good practice and understanding some new applications. J Exp Bot 64:3983–3998

    Article  CAS  PubMed  Google Scholar 

  44. Negri A, Brinkman D, Flores F, Botté E, Jones R, Webster N (2016) Acute ecotoxicology of natural oil and gas condensate to coral reef larvae. Sci Rep UK 21153

  45. Nyström M, Nordemar I, Tedengren M (2001) Simultaneous and sequential stress from increased temperature and copper on the metabolism of the hermatypic coral Porites cylindrica. Mar Biol 138:1225–1231

    Article  Google Scholar 

  46. Oliver LM, Fisher WS, Fore L, Smith A, Bradley P (2018) Assessing land use, sedimentation, and water quality stressors as predictors of coral reef condition in St. Thomas, U.S. Virgin Islands. Environ Monit Assess 190:213

  47. Paytan A, Mackey KRM, Chen Y, Lima ID, Doney SC, Mahowald N, Labiosa R, Post AF (2009) Toxicity of atmospheric aerosols on marine phytoplankton. Proc Natl Acad Sci 106:4601–4605

    Article  PubMed  Google Scholar 

  48. Potter SZ, Valentine JS (2003) The perplexing role of copper-zinc superoxide dismutase in amyotrophic lateral sclerosis (Lou Gehrig’s disease). J Biol Inorg Chem 8:373–380

    Article  CAS  PubMed  Google Scholar 

  49. Reichelt-Brushett AJ, Harrison PL (1999) The effect of copper, zinc and cadmium on fertilization success of gametes from scleractinian reef corals. Mar Pollut Bull 38:182–187

    Article  CAS  Google Scholar 

  50. Reichelt-Brushett AJ, Harrison PL (2000) The effect of copper on the settlement success of larvae from the scleractinian coral Acropora tenuis. Mar Pollut Bull 41:385–391

    Article  CAS  Google Scholar 

  51. Reichelt-Brushett AJ, McOrist G (2003) Trace metals in the living and nonliving components of scleractinian corals. Mar Pollut Bull 46:1573–1582

    Article  CAS  PubMed  Google Scholar 

  52. Reichelt-Brushett AJ, Harison PL (2005) The effect of selected trace metals on the fertilization success of several scleractinian coral species. Coral Reefs 24:524–534

    Article  Google Scholar 

  53. Reichelt-Brushett AJ, Michalek-Wagner K (2005) Effects of copper on the fertilization success of the soft coral Lobophytum compactum. Aquat Toxicol 74:280–284

    Article  CAS  PubMed  Google Scholar 

  54. Schwarz JA, Mitchelmore CL, Jones R, O’Dea A, Seymour S (2013) Exposure to copper induces oxidative and stress responses and DNA damage in the coral Montastraea franksi. Comp Biochem Physiol C Toxicol Pharmacol 157:272–279

    Article  CAS  PubMed  Google Scholar 

  55. Stimson J, Kinzie RA (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 153:63–74

    Article  Google Scholar 

  56. Tanaka K, Ohde S, Cohen MD, Snidvongs A, Ganmanee M, McLeod CW (2013) Metal contents of Porites corals from Khang Khao Island, Gulf of Thailand: Anthropogenic input of river runoff into a coral reef from urbanized areas, Bangkok. Appl Geochemistry 37:79–86

    Article  CAS  Google Scholar 

  57. Torfstein A, Teutsch N, Tirosh O, Shaked Y, Rivlin T, Zipori A, Stein M, Lazar B, Erel Y (2017) Chemical characterization of atmospheric dust from a weekly time series in the north Red Sea between 2006 and 2010. Geochim Cosmochim Acta 211:373–393

    Article  CAS  Google Scholar 

  58. Weis VM (2008) Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066

    Article  CAS  PubMed  Google Scholar 

  59. Wooldridge SA (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

    Article  CAS  PubMed  Google Scholar 

  60. Yruela I (2009) Copper in plants: Acquisition, transport and interactions. Funct Plant Biol 36:409–430

    Article  CAS  Google Scholar 

  61. Yruela I (2013) Transition metals in plant photosynthesis. Metallomics 5:1090

    Article  CAS  PubMed  Google Scholar 

  62. Zeng X, Chen X, Zhuang J (2015) The positive relationship between ocean acidification and pollution. Mar Pollut Bull 91:14–21

    Article  CAS  PubMed  Google Scholar 

  63. Zhou Z, Yu X, Tang J, Wu Y, Wang L, Huang B (2018) Systemic response of the stony coral Pocillopora damicornis against acute cadmium stress. Aquat Toxicol 194:132–139

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Dror Komet, Naama Kochman, Moty Ohevia and staff of the IUI for technical assistance. This study was funded in part by an Israel Science Foundation Grant (1794/16) to MF. On behalf of all authors, the corresponding author states that there is no conflict of interest.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Guilhem Banc-Prandi.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Topic Editor Morgan S. Pratchett

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 94 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Banc-Prandi, G., Fine, M. Copper enrichment reduces thermal tolerance of the highly resistant Red Sea coral Stylophora pistillata. Coral Reefs 38, 285–296 (2019). https://doi.org/10.1007/s00338-019-01774-z

Download citation

Keywords

  • Coral
  • Gulf of Aqaba
  • Thermo-tolerance
  • Copper
  • Climate change
  • Resistance