Skip to main content

Advertisement

SpringerLink
Log in

Juvenile Cassiopea andromeda medusae are resistant to multiple thermal stress events

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

Abstract

Oceans are undergoing successive heatwaves. Several invertebrate taxa associate with dinoflagellates and are susceptible to bleaching caused by heat stress. Although the impacts of a single bleaching event have been well documented, the consequences of successive events are less understood. We investigated the effects of multiple thermal stress events on juvenile Cassiopea andromeda, while also addressing the roles of symbiont concentration and heterotrophic diet regimen. We exposed medusae with two distinct symbiont concentrations (high and low) and under two feeding frequencies (Artemia offered daily and every 3 days) to three thermal stress events and at three temperatures (control of 27 °C, and treatments of 30 and 33 °C) while recording proportional changes in chlorophyll-a and jellyfish growth. Results show that 30 and 33 °C were not enough to trigger bleaching and did not affect growth. Symbiont concentration also did not affect growth, but medusae with higher symbiont concentration displayed higher chlorophyll-a loss. Diet regimen had little impact on chlorophyll-a variation, but had a dramatic effect on growth, as medusae fed daily grew, while those fed every 3 days shrank. These findings show that it is not possible to evaluate if C. andromeda becomes more resilient after successive thermal stress episodes, because even 33 °C did not generate enough stress. Therefore, C. andromeda juveniles are thermotolerant and may not serve as a good model for investigations on the resilience of coral reef zooxanthellate fauna to the current climate change predictions. Finally, at this life stage, the symbiotic relationship seems less important for growth than heterotrophy.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Similar content being viewed by others

References

  • Ainsworth TD, Heron SF, Ortiz JC, Mumby PJ, Grech A, Ogawa D, Eakin CM, Leggat W (2016) Climate change disables coral bleaching protection on the Great Barrier Reef. Science 352:338–342

    CAS  PubMed  Google Scholar 

  • Aljbour SM, Al-Horani FA, Kunzmann A (2018) Metabolic and oxidative stress responses of the jellyfish Cassiopea to pollution in the Gulf of Aqaba, Jordan. Mar Pollut Bull 130:271–278

    CAS  PubMed  Google Scholar 

  • Aljbour SM, Zimmer M, Al-Horani FA, Kunzmann A (2019) Metabolic and oxidative stress responses of the jellyfish Cassiopea sp. to changes in seawater temperature. J Sea Res 145:1–7

    Google Scholar 

  • Aljbour SM, Zimmer M, Kunzmann A (2017) Cellular respiration, oxygen consumption, and trade-offs of the jellyfish Cassiopea sp. in response to temperature change. J Sea Res 128:92–97

    Google Scholar 

  • 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

    Google Scholar 

  • Anthony KRN, Maynard JA, Diaz-Pulido G, Mumby PJ, Marshall PA, Cao L, Hoegh-Guldberg O (2011) Ocean acidification and warming will lower coral reef resilience. Glob Change Biol 17(5):1798–1808

    Google Scholar 

  • Armoza-Zvuloni R, Segal R, Kramarsky-Winter E, Loya Y (2011) Repeated bleaching events may result in high tolerance and notable gametogenesis in stony corals: Oculina patagonica as a model. Mar Ecol Prog Ser 426:149–159

    Google Scholar 

  • Bahr KD, Rodgers KUS, Jokiel PL (2017) Impact of three bleaching events on the reef resiliency of Kāne ‘ohe Bay, Hawai ‘i. Front Mar Sci 4:398

    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(4):435–471

    Google Scholar 

  • Battey JF, Patton JS (1986) Glycerol translocation in Condylactis gigantea. Mar Biol 95:37–46

    Google Scholar 

  • Berkelmans R (2009) Bleaching and mortality thresholds: how much is too much? In: van Oppen MJH, Lough JM (eds) Coral bleaching. Springer, Berlin, pp 103–119

    Google Scholar 

  • Cabrales-Arellano P, Islas-Flores T, Thomé PE, Villanueva MA (2017) Indomethacin reproducibly induces metamorphosis in Cassiopea xamachana scyphistomae. PeerJ 5:e2979

    PubMed  PubMed Central  Google Scholar 

  • Cantin NE, Cohen AL, Karnauskas KB, Tarrant AM, Mccorkle DC (2010) Ocean warming slows coral growth in the Central Red Sea. Science 329(5989):322–325

    CAS  PubMed  Google Scholar 

  • Çevik C, Erkol IL, Toklu B (2006) A new record of an alien jellyfish from the Levantine coast of Turkey - Cassiopea andromeda (Forsskål, 1775) [Cnidaria: Scyphozoa: Rhizostomeae]. Aquat Invasions 1(3):196–197

    Google Scholar 

  • Chaves-Fonnegra A, Riegl A, Zea S, Lopez JV, Smith T, Brandt M, Gilliam DS (2018) Bleaching events regulate shifts from corals to excavating sponges in algae-dominated reefs. Glob Change Biol 24(2):773–785

    Google Scholar 

  • Clayton WS Jr, Lasker HR (1984) Host feeding regimen and zooxanthellal photosynthesis in the anemone, Aiptasia pallida (Verrill). Biol Bull 167:590–600

    CAS  PubMed  Google Scholar 

  • Cunning R, Baker AC (2013) Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat Clim Chang 3(3):259–262

    Google Scholar 

  • Cunning R, Baker AC (2014) Not just who, but how many: the importance of partner abundance in reef coral symbioses. Front Microbiol 5:400

    PubMed  PubMed Central  Google Scholar 

  • Dawson MN, Martin LE, Penland LK (2001) Jellyfish swarms, tourists, and the Christ-child. In: Purcell JE, Graham WM, Dumont HJ (eds) Jellyfish blooms: ecological and societal importance. Springer, Dordrecht, pp 131–144

    Google Scholar 

  • De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci USA 109(44):17995–17999

    PubMed  Google Scholar 

  • Diaz JM, Hansel CM, Apprill A, Brighi C, Zhang T, Weber L, McNally S, Xun L (2016) Species-specific control of external superoxide levels by the coral holobiont during a natural bleaching event. Nat Commun 7:13801

    CAS  PubMed  PubMed Central  Google Scholar 

  • Djeghri N, Pondaven P, Stibor H, Dawson MN (2019) Review of the diversity, traits, and ecology of zooxanthellate jellyfishes. Mar Biol 166:147

    Google Scholar 

  • Ezzat L, Merle PL, Furla P, Buttler A, Ferrier-Pagès C (2013) The response of the Mediterranean gorgonian Eunicella singularis to thermal stress is independent of its nutritional regimen. PLoS ONE 8(5):e64370

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrier-Pagès C, Witting J, Tambutté E, Sebens KP (2003) Effect of natural zooplankton feeding on the tissue and skeletal growth of the scleractinian coral Stylophora pistillata. Coral Reefs 22(3):229–240

    Google Scholar 

  • Francini-Filho R, Reis R, Meirelle SP, Moura R, Thompson F, Kikuchi R, Kaufman L (2010) Seasonal prevalence of white plague like disease on the endemic Brazilian reef coral Mussismilia braziliensis. Lat Am J Aquat Res 38(2):292–296

    Google Scholar 

  • Freeman CJ, Stoner EW, Easson CG, Matterson KO, Baker DM (2016) Symbiont carbon and nitrogen assimilation in the Cassiopea-Symbiodinium mutualism. Mar Ecol Prog Ser 544:281–286

    CAS  Google Scholar 

  • Fu Z, Shibata M, Makabe R, Ikeda H, Uye SI (2014) Body size reduction under starvation, and the point of no return, in ephyrae of the moon jellyfish Aurelia aurita. Mar Ecol Prog Ser 510:255–263

    Google Scholar 

  • Glassom D (2014) Coral reefs and climate change. In: Freedman B (ed) Global environmental change. Springer, Dordrecht, pp 151–158

    Google Scholar 

  • Glynn PW (1983) Extensive “bleaching” and death of reef corals on the Pacific coast of Panama. Environ Conserv 10(2):149–154

    Google Scholar 

  • Glynn PW (1993) Coral reef bleaching: ecological perspectives. Coral Reefs 12(1):1–17

    Google Scholar 

  • Gold Z, Palumbi SR (2018) Long-term growth rates and effects of bleaching in Acropora hyacinthus. Coral Reefs 37(1):267–277

    Google Scholar 

  • Goreau T, McClanahan TR, Hayes R, Strong A (2000) Conservation of coral reefs after the 1998 bleaching event. Conserv Biol 14(1):5–15

    Google Scholar 

  • Graham NAJ (2014) Habitat complexity: coral structural loss leads to fisheries declines. Curr Biol 24(9):R359–R361

    CAS  PubMed  Google Scholar 

  • Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189

    CAS  PubMed  Google Scholar 

  • Grottoli AG, Warner ME, Levas SJ, Aschaffenburg MD, Schoepf V, McGinley M, Baumann J, Matsui Y (2014) The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Glob Change Biol 20(12):3823–3833

    Google Scholar 

  • Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50(8):839–866

    Google Scholar 

  • Hofmann DK, Fitt WK, Fleck J (1996) Checkpoints in the life-cycle of Cassiopea spp.: Control of metagenesis and metamorphosis in a tropical jellyfish. Int J Dev Biol 4(1):331–338

    Google Scholar 

  • Hogarth P (2015) The biology of mangroves and seagrasses, 3rd edn. Oxford University Press, Oxford

    Google Scholar 

  • Holland BS, Dawson MN, Crow L, Hofmann DK (2004) Global phylogeography of Cassiopea (Scyphozoa: Rhizostomeae): molecular evidence for cryptic species and multiple invasions of the Hawaiian Islands. Mar Biol 145:1119–1128

    Google Scholar 

  • Holm-Hansen O, Lorenzen CJ, Holmes RW, Strickland JD (1965) Fluorometric determination of chlorophyll. ICES J Mar Sci 30(1):3–15

    CAS  Google Scholar 

  • Houlbrèque F, Ferrier-Pagès C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev 84:1–17

    PubMed  Google Scholar 

  • Howells EJ, Abrego D, Meyer E, Kirk NL, Burt JA (2016) Host adaptation and unexpected symbiont partners enable reef-building corals to tolerate extreme temperatures. Glob Change Biol 22(8):2702–2714

    Google Scholar 

  • Hughes AD, Grottoli AG (2013) Heterotrophic compensation: a possible mechanism for resilience of coral reefs to global warming or a sign of prolonged stress? PLoS ONE 8(11):e81172

    PubMed  PubMed Central  Google Scholar 

  • Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JB, Kleypas J, Lough JM (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301(5635):929–933

    CAS  PubMed  Google Scholar 

  • Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis B (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17(4):360–365

    CAS  PubMed  Google Scholar 

  • Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin CM, Gilmour JP, Graham NAJ, Harrison H, Hobbs JA, Hoey AS, Hoogenboom M, Lowe RJ, McCulloch MT, Pandolfi JM, Pratchett M, Schoepf V, Torda G, Wilson SK (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 83:80–83

    Google Scholar 

  • Hughes TP, Kerry JT, Connolly SR, Baird AH, Eakin CM, Heron SF, Hoey AS, Hoogenboom MO, Jacobson M, Liu G, Pratchett MS, Skirving W, Torda G (2019) Ecological memory modifies the cumulative impact of recurrent climate extremes. Nat Clim Change 9:40–43

    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(21):10302–10305

    CAS  PubMed  Google Scholar 

  • IPCC (2014) Climate change 2014: Synthesis report. Contribution of Working Groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change [Core Writing Team, Pachauri RK, and Meyer LA (eds.)]. IPCC, Geneva, Switzerland

  • Klein SG, Pitta KA, Carroll AR (2016) Surviving but not thriving: inconsistent responses of zooxanthellate jellyfish polyps to ocean warming and future UV-B scenarios. Sci Rep 6:28859

    CAS  PubMed  PubMed Central  Google Scholar 

  • Klein SG, Pitt KA, Lucas CH, Hung SH, Schmidt-Roach S, Aranda M, Duarte CM (2019) Night-time temperature reprieves enhance the thermal tolerance of a symbiotic cnidarian. Front Mar Sci 6:453

    Google Scholar 

  • Knowlton N (2001) The future of coral reefs. Proc Natl Acad Sci USA 98:5419–5425

    CAS  PubMed  Google Scholar 

  • Kopp C, Domart-Coulon I, Barthelemy D, Meibom A (2016) Nutritional input from dinoflagellate symbionts in reef-building corals is minimal during planula larval life stage. Sci Adv 2:e1500681

    PubMed  PubMed Central  Google Scholar 

  • Kremer P (2005) Ingestion and elemental budgets for Linuche unguiculata, a scyphomedusa with zooxanthellae. J Mar Biol Assoc UK 85(3):613–625

    Google Scholar 

  • Krueger T, Hawkins TD, Becker S, Pontasch S, Dove S, Hoegh-Guldberg O, Leggat W, Fisher PL, Davy SK (2015) Differential coral bleaching-contrasting the activity and response of enzymatic antioxidants in symbiotic partners under thermal stress. Comp Biochem Physiol Part A Mol Integr Physiol 190:15–25

    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

    CAS  PubMed  Google Scholar 

  • Lampert KP (2016) Cassiopea and its zooxanthellae. In: Goffredo S, Dubinsky Z (eds) The cnidaria, past, present and future. Springer International Publishing, Switzerland, pp 415–423

    Google Scholar 

  • Leal MC, Ferrier-Pagès C, Petersen D, Osinga R (2017) Corals. In: Calado R, Olivotto I, Oliver MP, Holt GJ (eds) Marine ornamental species aquaculture. Wiley-Blackwell Publishing, UK, pp 406–436

    Google Scholar 

  • Lesser MP (1996) Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol Oceanogr 41(2):271–283

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Levas S, Grottoli AG, Schoepf V, Aschaffenburg M, Baumann J, Bauer JE, Warner ME (2016) Can heterotrophic uptake of dissolved organic carbon and zooplankton mitigate carbon budget deficits in annually bleached corals? Coral Reefs 35:495–506

    Google Scholar 

  • Manzello DP, Enochs IC, Kolodziej G, Carlton R, Valentino L (2018) Resilience in carbonate production despite three coral bleaching events in 5 years on an inshore patch reef in the Florida Keys. Mar Biol 165(6):99

    PubMed  PubMed Central  Google Scholar 

  • Marangoni LFDB, Mies M, Güth AZ, Banha TNS, Inague A, Fonseca JDS, Dalmolin C, Faria SC, Ferrier-Pagès C, Bianchini A (2019) Peroxynitrite generation and increased heterotrophic capacity are linked to the disruption of the coral-dinoflagellate symbiosis in a scleractinian and hydrocoral species. Microorganisms 7(10):426

    PubMed Central  Google Scholar 

  • McGill CJ, Pomory CM (2008) Effects of bleaching and nutrient supplementation on wet weight in the jellyfish Cassiopea xamachana (Bigelow) (Cnidaria: Scyphozoa). Mar Freshw Behav Physiol 41(3):179–189

    Google Scholar 

  • Meesters EH, Bak RPM (1993) Effects of coral bleaching on tissue regeneration potential and colony survival. Mar Ecol Prog Ser 96:189–198

    Google Scholar 

  • Mellas RE, McIlroy SE, Fitt WK, Coffroth MA (2014) Variation in symbiont uptake in the early ontogeny of the upside-down jellyfish, Cassiopea spp. J Exp Mar Biol Ecol 459:38–44

    Google Scholar 

  • Middlebrook R, Anthony KRN, Hoegh-Guldberg O, Dove S (2012) Thermal priming affects symbiont photosynthesis but does not alter bleaching susceptibility in Acropora millepora. J Exp Mar Biol Ecol 432–433:64–72

    Google Scholar 

  • Mies M, Chaves-Filho AB, Miyamoto S, Güth AZ, Tenório AA, Castro CB, Pires DO, Calderon EN, Sumida PYG (2017) Production of three symbiosis-related fatty acids by Symbiodinium types in clades A-F associated with marine invertebrate larvae. Coral Reefs 36:1319–1328

    Google Scholar 

  • Mies M, Güth AZ, Tenório AA, Banha TNS, Waters LG, Polito PS, Taniguchi S, Bícego MC, Sumida PYG (2018) In situ shifts of predominance between autotrophic and heterotrophic feeding in the reef-building coral Mussismilia hispida: an approach using fatty acid trophic markers. Coral Reefs 37(3):677–689

    Google Scholar 

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

    Google Scholar 

  • Morandini AC, Stampar SN, Maronna MM, da Silveira FL (2017) All non-indigenous species were introduced recently? The case study of Cassiopea (Cnidaria: Scyphozoa) in Brazilian waters. J Mar Biol Assoc UK 97(2):321–328

    Google Scholar 

  • Morrissey J, Sumich JL, Pinkard-Meier DR (2016) Introduction to the biology of marine life, 11th edn. Jones & Bartlett Learning, Burlington

    Google Scholar 

  • Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27(7):454–460

    Google Scholar 

  • Nesa B, Hidaka M (2009) High zooxanthellae density shortens the survival time of coral cell aggregates under thermal stress. J Exp Mar Biol Ecol 368(1):81–87

    Google Scholar 

  • Newkirk CR, Frazer TK, Martindale MQ (2018) Acquisition and proliferation of algal symbionts in bleached polyps of the upside-down jellyfish, Cassiopea xamachana. J Exp Mar Biol Ecol 508:44–51

    Google Scholar 

  • Newkirk CR, Frazer TK, Martindale MQ, Schnitzler CE (2020) Adaptation to bleaching: are thermotolerant Symbiodiniaceae strains more successful than other strains under elevated temperatures in a model symbiotic cnidarian? Front Microbiol 11:822

    PubMed  PubMed Central  Google Scholar 

  • Ohdera AH, Abrams MJ, Ames CL, Baker DM, Suescún-Bolívar LP, Collins AG, Freeman CJ, Gamero-Mora E, Goulet TL, Hofmann DK, Jaimes-Becerra A (2018) Upside-down but headed in the right direction: review of the highly versatile Cassiopea xamachana system. Front Ecol Evol 6:35

    Google Scholar 

  • Özgür E, Öztürk B (2008) A population of the alien jellyfish, Cassiopea andromeda (Forsskål, 1775) (Cnidaria: Scyphozoa: Rhizostomea) in the Ölüdeniz Lagoon. Turk Aquat Invas 3(4):423–428

    Google Scholar 

  • Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke RG, McArdle D, McClenachan L, Newman MJ, Paredes G, Warner RR, Jackson JB (2003) Global trajectories of the long-term of coral reef ecosystems. Science 301:955–958

    CAS  PubMed  Google Scholar 

  • Pierce J (2005) A system for mass culture of upside-down jellyfish Cassiopea spp as a potential food item for medusivores in captivity. Int Zoo Yearb 39(1):62–69

    Google Scholar 

  • Pitt KA (2000) Life history and settlement preferences of the edible jellyfish Catostylus mosaicus (Scyphozoa: Rhizostomeae). Mar Biol 136(2):269–279

    Google Scholar 

  • Pratchett MS, Bay LK, Gehrke PC, Koehn JD, Osborne K, Pressey RL, Sweatman HPA, Wachenfeld D (2011) Contribution of climate change to degradation and loss of critical fish habitats in Australian marine and freshwater environments. Mar Freshw Res 62(9):1062–1081

    Google Scholar 

  • Prieto L, Astorga D, Navarro G, Ruiz J (2010) Environmental control of phase transition and polyp survival of a massive-outbreaker jellyfish. PLoS ONE 5(11):e13793

    PubMed  PubMed Central  Google Scholar 

  • Roberty S, Fransolet D, Cardol P, Plumier JC, Franck F (2015) Imbalance between oxygen photoreduction and antioxidant capacities in Symbiodinium cells exposed to combined heat and high light stress. Coral Reefs 34(4):1063–1073

    Google Scholar 

  • Rocha RJ, Bontas B, Cartaxana P, Leal MC, Ferreira JM, Rosa R, Serôdio J, Calado R (2015) Development of a standardized modular system for experimental coral culture. J World Aquac Soc 46(3):235–251

    Google Scholar 

  • Roth MS (2014) The engine of the reef: photobiology of the coral-algal symbiosis. Front Microbiol 5:422

    PubMed  PubMed Central  Google Scholar 

  • Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265–269

    CAS  PubMed  Google Scholar 

  • Sachs JL, Wilcox TP (2006) A shift to parasitism in the jellyfish symbiont Symbiodinium microadriaticum. Proc R Soc B 273:425–429

    PubMed  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Schoepf V, Grottoli AG, Levas SJ, Aschaffenburg MD, Baumann JH, Matsui Y, Warner ME (2015) Annual coral bleaching and the long-term recovery capacity of coral. Proc R Soc B 282:20151887

    PubMed  Google Scholar 

  • Schubert P, Wilke T (2017) Coral Microcosms: challenges and opportunities for global change biology. In: Duque C (ed) Corals in a changing world. IntechOpen, London, pp 143–175

    Google Scholar 

  • Sheppard CRC, Davy SK, Pilling GM, Graham NAJ (2018) The biology of coral reefs, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Spalding MD, Ravilious C, Green EP (2001) World atlas of coral reefs. University of California Press, Berkeley

    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

    Google Scholar 

  • Stat M, Morris E, Gates RD (2008) Functional diversity in coral dinoflagellate symbiosis. Proc Natl Acad Sci USA 105(27):9256–9261

    CAS  PubMed  Google Scholar 

  • Stoner EW, Sebilian SS, Layman CA (2016) Comparison of zooxanthellae densities from upside-down jellyfish, Cassiopea xamachana, across coastal habitats of The Bahamas. Rev Biol Mar Oceanogr 51:203–208

    Google Scholar 

  • Swain TD, DuBois E, Gomes A, Stoyneva VP, Radosevich AJ, Henss J, Wagner ME, Derbas J, Grooms HW, Velazquez EM, Traub J, Kennedy BJ, Grigorescu AA, Westneat MW, Sanborn K, Levne S, Schick M, Parsons G, Biggs BC, Rogers JD, Backman V, Marcelino LA (2016) Skeletal light-scattering accelerates bleaching response in reef-building corals. BMC Ecol 16(1):10

    PubMed  PubMed Central  Google Scholar 

  • Swain TD, Chandler J, Backman V, Marcelino LA (2017) Consensus thermotolerance ranking for 110 Symbiodinium phylotypes: an exemplar utilization of a novel iterative partial-rank aggregation tool with broad application potential. Funct Ecol 31(1):172–183

    Google Scholar 

  • Tagliafico A, Rudd D, Rangel MS, Kelaher BP, Christidis L, Cowden K, Scheffers SR, Benkendorff K (2017) Lipid-enriched diets reduce the impacts of thermal stress in corals. Mar Ecol Prog Ser 573:129–141

    CAS  Google Scholar 

  • Tchernov D, Kvitt H, Haramaty L, Bibby TS, Gorbunov MY, Rosenfeld H, Falkowski PG (2011) Apoptosis and the selective survival of host animals following thermal bleaching in zooxanthellate corals. Proc Natl Acad Sci USA 108(24):9905–9909

    CAS  PubMed  Google Scholar 

  • Thé J, Barroso HS, Mammone M, Viana M, Batista CS, Mies M, Banha TNS, Morandini AC, Rossi S, Soares MO (2020) Aquaculture facilities promote populational stability throughout seasons and increase medusae size for the invasive jellyfish Cassiopea andromeda. Mar Environ Res 2020:105161

    Google Scholar 

  • Wasmund N, Topp I, Schories D (2006) Optimizing the storage and extraction of chlorophyll samples. Oceanologia 48(1):125–144

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and phaeopigments. Limnol Oceanogr 39(8):1985–1992

    CAS  Google Scholar 

  • Yakovleva IM, Baird AH, Yamamoto HH, Bhagooli R, Nonaka M, Hidaka M (2009) Algal symbionts increase oxidative damage. Mar Ecol Prog Ser 378:105–112

    CAS  Google Scholar 

Download references

Acknowledgements

We thank Mariana Andrade and the crew of Eco-Reef for helping during the experiments, Mayza Pompeu for technical assistance, Carla Zilberberg and Maurício Shimabukuro for their input on the manuscript, Linda Waters for reviewing the manuscript, and André Morandini for both reviewing the manuscript and assistance on identifications. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 1574760 and Eco-Reef Ltda.

Author information

Authors and Affiliations

  1. Instituto Oceanográfico, Universidade de São Paulo, São Paulo, SP, Brazil

    Thomás N. S. Banha, Miguel Mies, Arthur Z. Güth & Paulo Y. G. Sumida

  2. Department of Biology, University of West Florida, Pensacola, FL, USA

    Christopher M. Pomory

Authors
  1. Thomás N. S. Banha
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Miguel Mies
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Arthur Z. Güth
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christopher M. Pomory
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Paulo Y. G. Sumida
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

TNSB, MM, CMP, and PYGS designed the experiment; TNSB performed the experiments; MM and PYGS contributed with infrastructure/material/technical support; TNSB, MM, and AZG analyzed the data; all the authors contributed to the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Thomás N. S. Banha.

Ethics declarations

Conflict of interest

The authors state that there is no conflict of interest.

Ethics approval

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

Additional information

Responsible Editor: K. Bischof.

Publisher's Note

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

Reviewed by E. Stoner and undisclosed experts.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 470 kb)

Supplementary file2 (PDF 454 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Banha, T.N.S., Mies, M., Güth, A.Z. et al. Juvenile Cassiopea andromeda medusae are resistant to multiple thermal stress events. Mar Biol 167, 173 (2020). https://doi.org/10.1007/s00227-020-03792-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-020-03792-w

Search

Navigation