Skip to main content
SpringerLink
Log in

Sedimentation rapidly induces an immune response and depletes energy stores in a hard coral

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

High sedimentation rates have been linked to reduced coral health within multiple systems; however, whether this is a direct result of compromised coral immunity has not been previously investigated. The potential effects of sedimentation on immunity of the hard coral Montipora patula were examined by comparing physiological responses of coral fragments inoculated with sterilized marine sediments and those under control conditions. Sediments were collected from terrestrial runoff-affected reefs in SW Madagascar and applied cyclically for a total of 24 h at a rate observed during precipitation-induced sedimentation events. Coral health was determined 24 h after the onset of the sedimentation stress through measuring metabolic proxies of O2 budget and lipid ratios. Immune response of the melanin synthesis pathway was measured by quantifying phenoloxidase activity and melanin deposits. Sedimentation induced both immune and metabolic responses in M. patula. Both phenoloxidase activity and melanin deposition were significantly higher in the sediment treatment compared to controls, indicating an induced immune response. Sediment-treated corals also showed a tendency towards increased respiration (during the night) and decreased photosynthesis (during the day) and a significant depletion of energy reserves as compared to controls. These data highlight that short-term (24 h) sedimentation, free of live microorganisms, compromises the health of M. patula. The energetically costly immune response, potentially elicited by residual endotoxins and other inflammatory particles associated with the sterile sediments, likely contributes to the energy depletion. Overall, exposure to sedimentation adversely affects coral health and continued exposure may lead to resource depletion and an increased susceptibility to disease.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Anthony KRN (2006) Enhanced energy status of corals on coastal, high-turbidity reefs. Mar Ecol Prog Ser 319:111–116

    Article  Google Scholar 

  • Anthony K, Larcombe P (2000) Coral reefs in turbid waters: sediment-induced stresses in corals and likely mechanisms of adaptation. Proc 9th Int Coral Reef Symp 1:239-244

  • 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

  • Armitage SAO, Thompson JJW, Rolff J, Siva-Jothy MT (2003) Examining costs of induced and constitutive immune investment in Tenebrio molitor. J Evol Biol 16:1038–1044

    Article  CAS  PubMed  Google Scholar 

  • Burke L, Reytar K, Spalding M, Perry A (2011) Reefs at risk revisited. World Resources Institute, Washington, DC, USA

  • Cerenius L, Söderhäll K (2004) The prophenoloxidase-activating system in invertebrates. Immunol Rev 198:116–126

    Article  CAS  PubMed  Google Scholar 

  • Cerenius L, Kawabata SI, Lee BL, Nonaka M, Söderhäll K (2010) Proteolytic cascades and their involvement in invertebrate immunity. Trends Biochem Sci 35:575–583

    Article  CAS  PubMed  Google Scholar 

  • Cooper TF, Gilmour JP, Fabricius KE (2009) Bioindicators of changes in water quality on coral reefs: review and recommendations for monitoring programmes. Coral Reefs 28:589–606

    Article  Google Scholar 

  • Cotter SC, Wilson K (2002) Heritability of immune function in the caterpillar Spodoptera littoralis. Heredity 88:229–234

    Article  CAS  PubMed  Google Scholar 

  • Crossland CJ, Barnes DJ, Borowitzka MA (1980) Diurnal lipid and mucus production in the staghorn coral Acropora acuminata. Mar Biol 60:81–90

    Article  CAS  Google Scholar 

  • De’ath G, Fabricius K (2010) Water quality as a regional driver of coral biodiversity and macroalgae on the Great Barrier Reef. Ecol Appl 20:840–850

    Article  PubMed  Google Scholar 

  • Dubovskii IM, Grizanova EV, Chertkova EA, Slepneva IA, Komarov DA, Vorontsova YL, Glupov VV (2010) Generation of reactive oxygen species and activity of antioxidants in hemolymph of the moth larvae Galleria mellonella (L.) (Lepidoptera: Piralidae) at development of the process of encapsulation. J Evol Biochem Physiol 46:35–43

    Article  CAS  Google Scholar 

  • Erftemeijer PLA, Riegl B, Hoeksema BW, Todd PA (2012) Environmental impacts of dredging and other sediment disturbances on corals: A review. Mar Pollut Bull 64:1737–1765

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Feder D, Mello CB, Garcia ES, Azambuja P (1997) Immune responses in Rhodnius prolixus: influence of nutrition and ecdysone. J Insect Physiol 43:513–519

    Article  CAS  PubMed  Google Scholar 

  • Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:577–685

    Google Scholar 

  • Fitt WK, Gates RD, Hoegh-Guldberg O, Bythell JC, Jatkar A, Grottoli AG, Gomez M, Fisher P, Lajuenesse TC, Pantos O, Iglesias-Prieto R, Franklin DJ, Rodrigues LJ, Torregiani JM, van Woesik R, Lesser MP (2009) Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: The host does matter in determining the tolerance of corals to bleaching. J Exp Mar Bio Ecol 373:102–110

    Article  Google Scholar 

  • Flores F, Hoogenboom MO, Smith LD, Cooper TF, Abrego D, Negri AP (2012) Chronic exposure of corals to fine sediments: lethal and sub-lethal impacts. PLoS One 7:e37795

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Folch J, Lees M, Sloane Stanley G (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  • Grottoli AG, Rodrigues LJ, Juarez C (2004) Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event. Mar Biol 145:621–631

    Article  CAS  Google Scholar 

  • Haapkylä J, Unsworth RKF, Flavell M, Bourne DG, Schaffelke B, Willis BL (2011) Seasonal rainfall and runoff promote coral disease on an inshore reef. PLoS One 6:e16893

    Article  PubMed Central  PubMed  Google Scholar 

  • Harvell DC, Jordán-Dahlgren E, Merkel S, Rosenberg E, Raymundo L, Smith GW, Weil E, Willis BL (2007) Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography 20:172–195

    Article  Google Scholar 

  • Harvell DC, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, Hofmann EE, Lipp EK, Osterhaus ADME, Overstreet RM, Porter JW, Smith GW, Vasta GR (1999) Emerging marine diseases–climate links and anthropogenic factors. Science 285:1505–1510

    Article  CAS  PubMed  Google Scholar 

  • Heil M (2012) Damaged-self recognition as a general strategy for injury detection. Plant Signal Behav 7:576–580

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nyström M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    Article  CAS  PubMed  Google Scholar 

  • Kline DI, Kuntz NM, Breitbart M, Knowlton N, Rohwer F (2006) Role of elevated organic carbon levels and microbial activity in coral mortality. Mar Ecol Prog Ser 314:119–125

    Article  CAS  Google Scholar 

  • Lesser MP (2013) Using energetic budgets to assess the effects of environmental stress on corals: are we measuring the right things? Coral Reefs 32:25–33

    Article  Google Scholar 

  • Lirman D, Manzello D (2009) Patterns of resistance and resilience of the stress-tolerant coral Siderastrea radians (Pallas) to sub-optimal salinity and sediment burial. J Exp Mar Bio Ecol 369:72–77

    Article  Google Scholar 

  • Monroig Ó, Tocher DR, Navarro JC (2013) Biosynthesis of polyunsaturated fatty acids in marine invertebrates: recent advances in molecular mechanisms. Mar Drugs 11:3998–4018

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mydlarz LD, Palmer CV (2011) The presence of multiple phenoloxidases in Caribbean reef-building corals. Comp Biochem Physiol A Mol Integr Physiol 159:372–378

    Article  PubMed  Google Scholar 

  • Palmer CV, Traylor-Knowles N (2012) Towards an integrated network of coral immune mechanisms. Proc R Soc Lond B Biol Sci 279:4106–4114

    Article  CAS  Google Scholar 

  • Palmer CV, Mydlarz LD, Willis BL (2008) Evidence of an inflammatory-like response in non-normally pigmented tissues of two scleractinian corals. Proc R Soc Lond B Biol Sci 275:2687–2693

    Article  Google Scholar 

  • Palmer CV, Bythell JC, Willis BL (2010) Levels of immunity parameters underpin bleaching and disease susceptibility of reef corals. FASEB J 24:1935–1946

    Article  CAS  PubMed  Google Scholar 

  • Palmer CV, Bythell JC, Willis BL (2011a) A comparative study of phenoloxidase activity in diseased and bleached colonies of the coral Acropora millepora. Dev Comp Immunol 35:1098–1101

    Article  CAS  PubMed  Google Scholar 

  • Palmer CV, Traylor-Knowles NG, Willis BL, Bythell JC (2011b) Corals use similar immune cells and wound-healing processes as those of higher organisms. PLoS One 6:e23992

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Palmer CV, Bythell JC, Willis BL (2012) Enzyme activity demonstrates multiple pathways of innate immunity in Indo-Pacific anthozoans. Proc R Soc Lond B Biol Sci 279:3879–3887

    Article  CAS  Google Scholar 

  • Philipp E, Fabricius K (2003) Photophysiological stress in scleractinian corals in response to short-term sedimentation. J Exp Mar Bio Ecol 287:57–78

    Article  Google Scholar 

  • Piniak GA (2007) Effects of two sediment types on the fluorescence yield of two Hawaiian scleractinian corals. Mar Environ Res 64:456–468

    Article  CAS  PubMed  Google Scholar 

  • Raymundo LJ, Rosell KB, Reboton CT, Kaczmarsky L (2005) Coral diseases on Philippine reefs: genus Porites is a dominant host. Dis Aquat Org 64:181–191

    Article  PubMed  Google Scholar 

  • R Core Team (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL: http://www.R-project.org/

  • Reed K, Muller E, van Woesik R (2010) Coral immunology and resistance to disease. Dis Aquat Org 90:85–92

    Article  CAS  PubMed  Google Scholar 

  • Richardson LL (1997) Occurrence of the black band disease cyanobacterium on healthy corals of the Florida Keys. Bull Mar Sci 61:485–490

    Google Scholar 

  • Riegl B, Branch GM (1995) Effects of sediment on the energy budgets of four scleractinian (Bourne 1900) and five alcyonacean (Lamouroux 1816) corals. J Exp Mar Bio Ecol 186:259–275

    Article  Google Scholar 

  • Rock KL, Latz E, Ontiveros F, Kono H (2010) The sterile inflammatory response. Annu Rev Immunol 28:321–342

    Article  CAS  PubMed  Google Scholar 

  • Rogers CS (1990) Responses of coral reefs and reef organisms to sedimentation. Mar Ecol Prog Ser 62:185–202

    Article  Google Scholar 

  • Rossi F, Moisan M, Kong M, Laroussi M (2012) Special issue on plasma sterilization and decontamination. Plasma Process Polym 9:559–560

    Article  CAS  Google Scholar 

  • Saunders SM, Radford B, Bourke SA, Thiele Z, Bech T, Mardon J (2005) A rapid method for determining lipid fraction ratios of hard corals under varying sediment and light regimes. Environ Chem 2:331–336

    Article  CAS  Google Scholar 

  • Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc R Soc Lond B Biol Sci 270:357–366

    Article  Google Scholar 

  • Seeman J, Carballo–Bolaños R, Berry KL, González CT, Richter C, Leinfelder RR (2012) Importance of heterotrophic adaptations of corals to maintain energy reserves. Proc 12th Int Coral Reef Symp, 19:9–13

  • Seppälä O, Liljeroos K, Karvonen A, Jokela J (2008) Host condition as a constraint for parasite reproduction. Oikos 117:749–753

    Article  Google Scholar 

  • Stafford-Smith M, Ormond R (1992) Sediment-rejection mechanisms of 42 species of Australian scleractinian corals. Mar Freshw Res 43:683–705

    Article  Google Scholar 

  • Stedman (2000) Stedman’s medical dictionary. Williams and Wilkins, Baltimore, MD, USA

    Google Scholar 

  • Storlazzi CD, Field ME, Bothner MH (2011) The use (and misuse) of sediment traps in coral reef environments: theory, observations, and suggested protocols. Coral Reefs 30:23–38

    Article  Google Scholar 

  • Sugumaran M (2002) Comparative biochemistry of eumelanogenesis and the protective roles of phenoloxidase and melanin in insects. Pigment Cell Res 15:2–9

    Article  CAS  PubMed  Google Scholar 

  • Suzuki A, Kawahata H, Tanimoto Y, Tsukamoto H, Gupta LP, Yukino I (2000) Skeletal isotopic record of a Porites coral during the 1998 mass bleaching event. Geochem J 34:321–329

    Article  CAS  Google Scholar 

  • Szmant AM, Gassman NJ (1990) The effects of prolonged “bleaching” on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 8:217–224

    Article  Google Scholar 

  • Vanderplanck M, Michez D, Vancraenenbroeck S, Lognay G (2011) Micro-quantitative method for analysis of sterol levels in honeybees and their pollen loads. Anal Lett 44:1807–1820

    Article  CAS  Google Scholar 

  • Voss JD, Richardson LL (2006) Coral diseases near Lee Stocking Island, Bahamas: patterns and potential drivers. Dis Aquat Org 69:33–40

    Article  PubMed  Google Scholar 

  • Ward S (1995) The effect of damage on the growth, reproduction and storage of lipids in the scleractinian coral Pocillopora damicornis (Linnaeus). J Exp Mar Bio Ecol 187:193–206

    Article  CAS  Google Scholar 

  • Weber M, Lott C, Fabricius KE (2006) Sedimentation stress in a scleractinian coral exposed to terrestrial and marine sediments with contrasting physical, organic and geochemical properties. J Exp Mar Bio Ecol 336:18–32

    Article  CAS  Google Scholar 

  • Weber M, de Beer D, Lott C, Polerecky L, Kohls K, Abed RMM, Ferdelman TG, Fabricius KE (2012) Mechanisms of damage to corals exposed to sedimentation. Proc Natl Acad Sci USA 109:E1558–E1567

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Williams GJ, Aeby GS, Cowie ROM, Davy SK (2010) Predictive modeling of coral disease distribution within a reef system. PLoS One 5:e9264

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

Funding for this project was obtained from the National Fund for Scientific Research (FNRS F3/5/5-A2/5-MCF/DM-A115), Leopold III Funds, and the Agence Francophone pour l’Education (AEF). We would like to thank Antoigne Patiny for his help with the design and preparation of the inoculation experiment, Maryse Vanderplank and Georges Lognay for their help with lipid extraction procedures, and JM Baele for his help with sediment analyses. This study is a contribution of the Centre Interuniversitaire de Biologie Marine and the Polyaquaculture Research Unit. We would also like to thank the editors and two anonymous reviewers for their useful comments.

Author information

Authors and Affiliations

  1. Biology of Marine Organisms and Biomimetics Lab, Pentagone 2B, Research Institute for Biosciences, University of Mons, Avenue du champ de Mars 6, 7000, Mons, Belgium

    C. Sheridan & I. Eeckhaut

  2. Numerical Ecology of Aquatic Systems Lab, University of Mons, Avenue du champ de Mars 6, 7000, Mons, Belgium

    Ph. Grosjean & J. Leblud

  3. School of Biological Sciences, Plymouth University, Drake Circus, Plymouth, Devon, PL4 8AA, UK

    C. V. Palmer

  4. Avram and Stella Goldstein-Goren Department of Biotechnology Engineering, The National Institute for Biotechnology in the Negev (NIBN), Ben-Gurion University of the Negev, P.O. Box 653, 84105, Beersheba, Israel

    A. Kushmaro

  5. School of Materials Science and Engineering, Nanyang Technological University, Singapore, Singapore

    A. Kushmaro

  6. Polyaquaculture Research Unit, IH.SM, Toliara, Madagascar

    I. Eeckhaut

Authors
  1. C. Sheridan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ph. Grosjean
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Leblud
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. V. Palmer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. Kushmaro
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. I. Eeckhaut
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. Sheridan.

Additional information

Communicated by Biology Editor Dr. Ruth Gates

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sheridan, C., Grosjean, P., Leblud, J. et al. Sedimentation rapidly induces an immune response and depletes energy stores in a hard coral. Coral Reefs 33, 1067–1076 (2014). https://doi.org/10.1007/s00338-014-1202-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-014-1202-x

Keywords

Search

Navigation