Skip to main content

Advertisement

SpringerLink
Log in

Bleaching in reef invertebrate larvae associated with Symbiodinium strains within clades A–F

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Coral reefs are diverse ecosystems relying on the presence of dinoflagellates (genus Symbiodinium), that are found in symbiotic association with multiple phyla and performing the majority of primary production. However, coral reefs are currently threatened by climate change and the increase in seawater temperature, which causes the bleaching phenomenon. While bleaching has been well documented for adult host organisms, it is still poorly understood in larval stages. We offered Symbiodinium types within clades A–F to the larvae of Mussismilia hispida (scleractinian coral), Berghia stephanieae (nudibranch) and Tridacna crocea (giant clam) and manipulated the temperature to 26, 29 or 32 °C. Samples were taken at 0, 12, 24, 48 and 72 h post-temperature increase, chlorophyll-a (chl-a) was extracted and its content measured in a fluorometer. Symbiodinium type, temperature and time all influenced chl-a content. M. hispida larvae displayed a bleaching threshold at 29 °C; larvae containing Symbiodinium A–F all bleached at 32 °C, but with significantly lower bleaching in larvae associated with type A1. B. stephanieae digested the symbionts; while chl-a content decreased over time equally for all clades, it is not possible to determine if it is related to bleaching. T. crocea larvae at 29 °C bleached for all symbiont types, except for A1. At 32 °C, all types were bleached, but type A1 bleached significantly less. These findings show that type A1 seems to be more thermo-tolerant in larvae of the tested species. This may be related to the fact that strains within this clade are homologous to both M. hispida and T. crocea, as they are found within these adult host’ tissues. Therefore, symbiont type may have an important role in invertebrate larvae development and present relevant implications for recruitment.

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

Similar content being viewed by others

References

  • Abrego D, van Oppen MJH, Willis BL (2009) Highly infectious symbiont dominates initial uptake in coral juveniles. Mol Ecol 18:3518–3531

    Article  Google Scholar 

  • Albright R, Mason B, Miller M, Langdon C (2010) Ocean acidification compromises recruitment success of the threatened Caribbean coral Acropora palmata. Proc Natl Acad Sci USA 107:20400–20404

    Article  CAS  Google Scholar 

  • Allemand D, Furla P, Bénazet-Tambutté S (1998) Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Can J Bot 76:925–941

    CAS  Google Scholar 

  • Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689

    Article  Google Scholar 

  • Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar Coast Shelf Sci 80:435–471

    Article  Google Scholar 

  • Barneah O, Brickner I, Hooge M et al (2007) Three party symbiosis: acoelomorph worms, corals and unicellular algal symbionts in Eilat (Red Sea). Mar Biol 151:1215–1223

    Article  Google Scholar 

  • Belda-Baillie CA, Sison M, Silvestre V et al (1999) Evidence for changing symbiotic algae in juvenile tridacnids. J Exp Mar Biol Ecol 241:207–221

    Article  Google Scholar 

  • Brander LM, Van Beukering P, Cesar HSJ (2007) The recreational value of coral reefs: a meta-analysis. Ecol Econom 63:209–218

    Article  Google Scholar 

  • Brown BE (1997) Adaptations of reef corals to physical environmental stress. Adv Mar Biol 31:221–299

    Article  Google Scholar 

  • Carlos AA, Baillie BK, Maruyama T (2000) Diversity of dinoflagellate symbionts (zooxanthellae) in a host individual. Mar Ecol Prog Ser 195:93–100

    Article  Google Scholar 

  • Carroll DJ, Kempf SC (1990) Laboratory culture of the aeolid nudibranch Berghia verrucicornis (Mollusca, Opisthobranchia): some aspects of its development and life history. Biol Bull 179:243–253

    Article  CAS  Google Scholar 

  • Cesar HS (2000) Coral reefs: their functions, threats and economical value. In: Cesar HS (ed) Collected Essays on the Economics of Coral Reefs. Cordio, Kalmar, pp 14–39

    Google Scholar 

  • Chen CA, Lam KK, Nakano Y, Tsai WS (2003) A stable association of the stress-tolerant zooxanthellae, Symbiodinium clade D, with the low-temperature-tolerant coral, Oulastrea crispata (Scleractinia: Faviidae) in subtropical non-reefal coral communities. Zool Stud 42:540–550

    Google Scholar 

  • Colombo-Pallotta MF, Rodríguez-Román A, Iglesias-Prieto R (2010) Calcification in bleached and unbleached Montastraea faveolata: evaluating the role of oxygen and glycerol. Coral Reefs 29:899–907

    Article  Google Scholar 

  • Cooper TF, Ulstrup KE, Dandan SS et al (2011) Niche specialization of reef-building corals in the mesophotic zone: metabolic trade-offs between divergent Symbiodinium types. Proc R Soc B 278:1840–1850

    Article  Google Scholar 

  • Cumbo VR, Baird AH, van Oppen MJH (2012) The promiscuous larvae: flexibility in the establishment of symbiosis in corals. Coral Reefs 32:111–120

    Article  Google Scholar 

  • Cumbo VR, Fan TY, Edmunds PJ (2013) Effects of exposure duration on the response of Pocillopora damicornis larvae to elevated temperature and high pCO2. J Exp Mar Biol Ecol 439:100–107

    Article  Google Scholar 

  • De Lima LA, Migliolo L, Castro CBE et al (2013) Identification of a novel antimicrobial peptide from Brazilian coast coral Phyllogorgia dilatata. Protein Pept Lett 20:1153–1158

    Article  Google Scholar 

  • DeBoer TS, Baker AC, Erdmann MV et al (2012) Patterns of Symbiodinium distribution in three giant clam species across the biodiverse Bird’s Head region of Indonesia. Mar Ecol Prog Ser 444:117–132

    Article  CAS  Google Scholar 

  • Edmunds PJ, Gates RD, Leggat W et al (2005) The effect of temperature on the size and population density of dinoflagellates in larvae of the reef coral Porites astreoides. Invertebr Biol 124:185–193

    Article  Google Scholar 

  • Fitt WK, Spero HJ, Halas J et al (1993) Recovery of the coral Montastrea annularis in the Florida keys after the 1987 Caribbean “bleaching event”. Coral Reefs 12:57–64

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Furla P, Allemand D, Shick JM, Ferrier-Pagès C, Richier S, Plantivaux A, Merle PL, Tambutté S (2005) The symbiotic anthozoan: a physiological chimera between alga and animal. Integr Comp Biol 45:595–604

    Article  CAS  Google Scholar 

  • Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Global Change Biol 2:495–509

    Article  Google Scholar 

  • Grant AJ, Rémond M, People J, Hinde R (1997) Effects of host-tissue homogenate of the scleractinian coral Plesiastrea versipora on glycerol metabolism in isolated symbiotic dinoflagellates. Mar Biol 128:665–670

    Article  CAS  Google Scholar 

  • Guillard RR, Ryther JH (1962) Studies of marine planktonic diatoms, I: Cycotella nana hustedl, and Detonula confervacea (cleve) gran. Can J Microbiol 8:229–239

    Article  CAS  Google Scholar 

  • Haryanti D, Yasuda N, Harii S, Hidaka M (2015) High tolerance of symbiotic larvae of Pocillopora damicornis to thermal stress. Zool Stud 54:52

    Article  Google Scholar 

  • Heslinga GA, Watson TC, Isamu T (1990) Giant clam farming. Pacific Fisheries Development Foundation (NMFS/NOAA), Honolulu

    Google Scholar 

  • Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshwater Res 50:839–866

    Article  Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ et al (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  CAS  Google Scholar 

  • Hughes TP, Baird AH, Bellwood DR et al (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    Article  CAS  Google Scholar 

  • Hughes TP, Rodrigues MJ, Bellwood DR et al (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17:360–365

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Jokiel PL, Rodgers KS, Kuffner IB et al (2008) Ocean acidification and calcifying reef organisms: a mesocosm investigation. Coral Reefs 27:473–483. https://doi.org/10.1007/s00338-008-0380-9

    Article  Google Scholar 

  • 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. https://doi.org/10.1046/j.1365-3040.1998.00345.x

    Article  CAS  Google Scholar 

  • Knowlton N, Brainard RE, Fisher R et al (2010) Coral reef biodiversity. In: McIntyre AD (ed) Life in the world’s oceans: diversity, distribution, and abundance. Blackwell Publishing, Oxford, pp 65–77

    Chapter  Google Scholar 

  • Ladner JT, Barshis DJ, Palumbi SR (2012) Protein evolution in two co-occurring types of Symbiodinium: an exploration into the genetic basis of thermal tolerance in Symbiodinium clade D. BMC Evol Biol 12:217

    Article  CAS  Google Scholar 

  • LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull 199:126–134

    Article  CAS  Google Scholar 

  • Leal MC, Nunes C, Alexandre D et al (2012) Parental diets determine the embryonic fatty acid profile of the tropical nudibranch Aeolidiella stephanieae: the effect of eating bleached anemones. Mar Biol 159:1745–1751

    Article  CAS  Google Scholar 

  • Leal MC, Ferrier-Pagès C, Petersen D, Osinga R (2017) Corals. Wiley-Blackwell Publishing, United Kingdom

    Book  Google Scholar 

  • Leggat W, Buck BH, Grice A, Yellowlees D (2003) The impact of bleaching on the metabolic contribution of dinoflagellate symbionts to their giant clam host. Plant, Cell Environ 26:1951–1961

    Article  CAS  Google Scholar 

  • Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278

    Article  CAS  Google Scholar 

  • Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494

    Article  CAS  Google Scholar 

  • Lohbeck KT, Riebesell U, Reusch TBH (2012) Adaptive evolution of a key phytoplankton species to ocean acidification. Nat Geosci 5:346–351. https://doi.org/10.1038/ngeo1441

    Article  CAS  Google Scholar 

  • McGinty ES, Pieczonka J, Mydlarz LD (2012) Variations in reactive oxygen release and antioxidant activity in multiple Symbiodinium types in response to elevated temperature. Microb Ecol 64:1000–1007

    Article  CAS  Google Scholar 

  • Mieog JC, Olsen JL, Berkelmans R et al (2009) The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS ONE 4:e6364

    Article  Google Scholar 

  • Mies M, Sumida PYG (2012) Giant clam aquaculture: a review on induced spawning and larval rearing. Int J Mar Sci 2:62–69

    Google Scholar 

  • Mies M, Braga F, Scozzafave MS et al (2012) Early development, survival and growth rates of the giant clam Tridacna crocea (Bivalvia: Tridacnidae). Braz J Oceanogr 60:129–135

    Article  Google Scholar 

  • Mies M, Chaves-Filho AB, Miyamoto S, Güth AZ, Tenório AA, Castro CB, Pires DO, Calderon EN, Sumida PYG (2017a) Production of three symbiosis-related fatty acids by Symbiodinium types in clades A-F associated with marine invertebrate larvae. Coral Reefs. https://doi.org/10.1007/s00338-017-1627-0

    Google Scholar 

  • Mies M, Voolstra CR, Castro CB et al (2017b) Expression of a symbiosis-specific gene in Symbiodinium type A1 associated with coral, nudibranch and giant clam larvae. R Soc Open Sci 4:170253. https://doi.org/10.1098/rsos.170253

    Article  CAS  Google Scholar 

  • Moberg F, Folke C (1999) Ecological goods and services of coral reef ecosystems. Ecol Econom 29:215–233

    Article  Google Scholar 

  • Morse ANC, Iwao K, Baba M et al (1996) An ancient chemosensory mechanism new life to coral reefs. Biol Bull 191:149–154

    Article  Google Scholar 

  • Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in coral reefs. In: Dubinsky Z (ed) Ecosystems of the World. Elsevier, Amsterdam, pp 75–87

    Google Scholar 

  • Nesa B, Baird AH, Harii S et al (2012) Algal symbionts increase DNA damage in coral planulae exposed to sunlight. Zool Stud 51:12–17

    CAS  Google Scholar 

  • Neves EG, Pires DO (2002) Sexual reproduction of Brazilian coral Mussismilia hispida (Verrill, 1902). Coral Reefs 21:161–168

    Google Scholar 

  • Newton K, Côté IM, Pilling GM et al (2007) Current and future sustainability of island coral reef fisheries. Curr Biol 17:655–658

    Article  CAS  Google Scholar 

  • Olivotto I, Planas M, Simões N et al (2011) Advances in breeding and rearing marine ornamentals. J World Aquac Soc 42:135–166

    Article  Google Scholar 

  • Pandolfi JM, Bradbury RH, Sala E et al (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955–958

    Article  CAS  Google Scholar 

  • Picciani N, Seiblitz IGL, de Paiva PC et al (2016) Geographic patterns of Symbiodinium diversity associated with the coral Mussismilia hispida (Cnidaria, Scleractinia) correlate with major reef regions in the Southwestern Atlantic Ocean. Mar Biol. https://doi.org/10.1007/s00227-016-3010-z

    Google Scholar 

  • Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Mol Phylogenet Evol 56:492–497

    Article  CAS  Google Scholar 

  • Porter JW, Fitt WK, Spero HJ et al (1989) Bleaching in reef corals: Physiological and stable isotopic responses. Proc Natl Acad Sci USA 86:9342–9346. https://doi.org/10.1073/pnas.86.23.9342

    Article  CAS  Google Scholar 

  • Ralph PJ, Larkum AWD, Kühl M (2005) Temporal patterns in effective quantum yield of individual zooxanthellae expelled during bleaching. J Exp Mar Biol Ecol 316:17–28

    Article  Google Scholar 

  • Rowan R, Powers DA (1991) Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar Ecol Prog Ser 71:65–73

    Article  CAS  Google Scholar 

  • Schnitzler CE, Hollingsworth LL, Krupp DA, Weis VM (2012) Elevated temperature impairs onset of symbiosis and reduces survivorship in larvae of the Hawaiian coral, Fungia scutaria. Mar Biol 159:633–642

    Article  Google Scholar 

  • Sheppard CRC, Davy SK, Pilling GM (2009) The biology of coral reefs. Oxford University Press, Oxford

    Book  Google Scholar 

  • Stat M, Carter D, Hoegh-Guldberg O (2006) The evolutionary history of Symbiodinium and scleractinian hosts—symbiosis, diversity, and the effect of climate change. Perspect Plant Ecol Evol Syst 8:23–43

    Article  Google Scholar 

  • Strychar KB, Coates M, Sammarco PW et al (2005) Loss of Symbiodinium from bleached soft corals Sarcophyton ehrenbergi, Sinularia sp. and Xenia sp. J Exp Mar Biol Ecol 320:159–177

    Article  Google Scholar 

  • van Oppen MJH, Mahiny AJ, Done TJ (2005) Geographic distribution of zooxanthella types in three coral species on the great barrier reef sampled after the 2002 bleaching event. Coral Reefs 24:482–487

    Article  Google Scholar 

  • Venn AA, Wilson MA, Trapido-Rosenthal HG et al (2006) The impact of coral bleaching on the pigment profile of the symbiotic alga, Symbiodinium. Environment 29:2133–2142

    CAS  Google Scholar 

  • Venn AA, Loram JE, Douglas AE (2008) Photosynthetic symbioses in animals. J Exp Bot 59:1069–1080

    Article  CAS  Google Scholar 

  • Vermeij MJA, Frade PR, Bak RPM (2013) Zooxanthellae presence acts as a settlement cue for aposymbiotic planulae of the caribbean coral Montastraea faveolata. Caribb J Sci 47:31–36

    Article  Google Scholar 

  • Warner WK, Fitt WK, Schmidt GW (1996) The effects of elevated temperature on the photosynthetic efficiency of zooxantheliae in hospite from four different species of reef coral: a novel approach. Plant, Cell Environ 19:291–299

    Article  Google Scholar 

  • Wasmund N, Topp I, Schories D (2006) Optimising the storage and extraction of chlorophyll samples. Oceanologia 48:125–144

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Weis VM, Reynolds WS, DeBoer MD, Krupp DA (2001) Host-symbiont specificity during onset of symbiosis between the dinoflagellates Symbiodinium spp. and planula larvae of the scleractinian coral Fungia scutaria. Coral Reefs 20:301–308

    Article  Google Scholar 

  • Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39:1985–1992

    Article  CAS  Google Scholar 

  • Winter APM, Chaloub RM, Duarte GAS, Castro CB (2016) Photosynthetic responses of corals Mussismilia harttii (Verrill, 1867) from turbid waters to changes in temperature and presence/absence of light. Braz J Oceanogr 64:203–216

    Article  Google Scholar 

  • Yakovleva IM, Baird AH, Yamamoto HH et al (2009) Algal symbionts increase oxidative damage and death in coral larvae at high temperatures. Mar Ecol Prog Ser 378:105–112

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Linda Waters, Stephen Kempf and William Fitt for kindly reviewing the manuscript and providing important notes. We also thank Mary Alice Coffroth and the Buffalo Undersea Reef Research Collection for supplying the Symbiodinium cultures, Flávia Saldanha-Corrêa for maintaining them, the Coral Vivo Institute staff, and Salvador Gaeta for the use of his facilities and equipment. This work was supported by Projeto Coral Vivo and sponsored by Petrobras and Arraial d’Ajuda Eco Parque. PYGS acknowledges Grants 302526/2012-9 and 2010/20350-8 from CNPq and FAPESP.

Author information

Authors and Affiliations

  1. Oceanographic Institute, University of São Paulo (IO-USP), Praça do Oceanográfico, 191 - Cidade Universitária, São Paulo, SP, 05508-120, Brazil

    M. Mies, A. Z. Güth, M. Pompeu & P. Y. G. Sumida

  2. Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, s/n, Rio de Janeiro, RJ, 20940-040, Brazil

    C. B. Castro & D. O. Pires

  3. Instituto Coral Vivo, Rua dos Coqueiros 87, Santa Cruz Cabrália, BA, 45807-000, Brazil

    C. B. Castro, D. O. Pires & E. N. Calderon

  4. Núcleo em Ecologia e Desenvolvimento Socioambiental de Macaé, Universidade Federal do Rio de Janeiro, Av São José do Barreto 764, Macaé, RJ, 27965-045, Brazil

    E. N. Calderon

Authors
  1. M. Mies
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Z. Güth
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. B. Castro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. O. Pires
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. E. N. Calderon
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. Pompeu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. P. Y. G. Sumida
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MM designed the experiment, MM performed the experiment, CBC, DOP, ENC, MP and PYGS contributed with infrastructure/material/technical support, MM and AZG analyzed the data and MM and PYGS wrote the manuscript.

Corresponding author

Correspondence to M. Mies.

Ethics declarations

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Conflict of interest

The authors have no conflict of interest.

Additional information

Responsible Editor: R. Hill.

Reviewed by C. Zilberberg and an undisclosed expert.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mies, M., Güth, A.Z., Castro, C.B. et al. Bleaching in reef invertebrate larvae associated with Symbiodinium strains within clades A–F. Mar Biol 165, 6 (2018). https://doi.org/10.1007/s00227-017-3263-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-017-3263-1

Search

Navigation