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The giant clam Tridacna squamosa quickly regenerates iridocytes and restores symbiont quantity and phototrophic potential to above-control levels in the outer mantle after darkness-induced bleaching

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Abstract

Giant clams are ecologically and economically relevant reef inhabitants that host photosynthetic dinoflagellates inside tubules located mainly in their colorful outer mantle. This study examined the effects of exposure to darkness for 30 days and the subsequent 11 days of recovery under a normal photoperiod on the outer mantle of the fluted giant clam Tridacna squamosa. Changes in the abundance of iridocytes and symbionts were assessed by fluorescence microscopy. Light microscopy was applied to quantify symbionts isolated from the outer mantle, while chlorophyll was extracted and analyzed by spectroscopy. The transcript levels of the host’s vacuolar-type H+-ATPase subunit A (ATP6V1A) and symbionts’ form II ribulose-1,5-bisphosphate carboxylase/oxygenase (Zoox-rbcII) were determined by quantitative real-time PCR (qPCR) and used as proxies for iridocyte abundance and phototrophic potential, respectively. The protein abundance of ATP6V1A and Zoox-RBCII was quantified by western blotting. After exposure to darkness for 30 days, the outer mantle of T. squamosa individuals lost the distinct multiple color patterns, and the gene and protein expression levels of ATP6V1A/ATP6V1A and Zoox-rbcII/Zoox-RBCII decreased dramatically. Microscopy assessment confirmed the reduction in iridocyte and symbiont populations, and the chlorophyll level also decreased considerably. However, just 11 days after returning to a normal light:dark regimen, the quantity of coccoid dinoflagellates and the expression of Zoox-rbcII/Zoox-RBCII in the outer mantle increased significantly to levels higher than those of the individuals prior to exposure to darkness (control), while the chlorophyll content returned to the control level. Additionally, the outer mantle regained most of its coloration with partial recovery of the iridocyte population. These results are relevant not only for understanding the phenomena of light deprivation and symbiont loss in dinoflagellate-associated reef organisms, but also signify that the giant clam-coccoid dinoflagellate holobiont is phototrophically plastic and particularly tolerant to bleaching.

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References

  • Addessi L (2001) Giant clam bleaching in the lagoon of Takapoto atoll (French Polynesia). Coral Reefs 19:220–220

    Google Scholar 

  • Andréfouët S, Van Wynsberge S, Gaertner-Mazouni N, Menkes C, Gilbert A, Remoissenet G (2013) Climate variability and massive mortalities challenge giant clam conservation and management efforts in French Polynesia atolls. Biol Cons 160:190–199

    Google Scholar 

  • Barshis DJ, Ladner JT, Oliver TA, Seneca FO, Traylor-Knowles N, Palumbi SR (2013) Genomic basis for coral resilience to climate change. PNAS 110:1387–1392. https://doi.org/10.1073/pnas.1210224110

    Article  PubMed  PubMed Central  Google Scholar 

  • Brading P, Warner ME, Davey P, Smith DJ, Achterberg EP, Suggett DJ (2011) Differential effects of ocean acidification on growth and photosynthesis among phylotypes of Symbiodinium (Dinophyceae). Limnol Oceanogr 56:927–938

    CAS  Google Scholar 

  • Buck BH, Rosenthal H, Saint-Paul U (2002) Effect of increased irradiance and thermal stress on the symbiosis of Symbiodinium microadriaticum and Tridacna gigas. Aquat Living Resour 15:107–117

    Google Scholar 

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

    Google Scholar 

  • Chan CYL, Hiong KC, Boo MV, Choo CYL, Wong WP, Chew SF, Ip YK (2018) Light exposure enhances urea absorption in the fluted giant clam, Tridacna squamosa, and up-regulates the protein abundance of a light-dependent urea active transporter, DUR3-like, in its ctenidium. J Exp Biol 221:jeb176313. https//doi.org/https://doi.org/10.1242/jeb.176313

  • Chan CYL, Hiong KC, Choo CYL, Boo MV, Wong WP, Chew SF, Ip YK (2019) Increased apical sodium-dependent glucose transporter abundance in the ctenidium of the giant clam Tridacna squamosa upon illumination. J Exp Biol 222:jeb195644. https//doi.org/https://doi.org/10.1242/jeb.195644

  • Chan CYL, Hiong KC, Choo CYL, Boo MV, Wong WP, Chew SF, Ip YK (2020) Light-enhanced phosphate absorption in the fluted giant clam, Tridacna squamosa, entails an increase in the expression of sodium-dependent phosphate transporter 2a in its colorful outer mantle. Coral Reefs 39:1055–1070. https://doi.org/10.1007/s00338-020-01930-w

    Article  Google Scholar 

  • Chew SF, Koh CZY, Hiong KC, Boo MV, Wong WP, Ip YK (2020) The fluted giant clam (Tridacna squamosa) increases the protein abundance of the host’s copper-zinc superoxide dismutase in the colorful outer mantle, but not the whitish inner mantle, during light exposure. Comp Biochem Physiol A 250:110791. https://doi.org/10.1016/j.cbpa.2020.110791

    Article  CAS  Google Scholar 

  • Costanza R, De Groot R, Sutton P, Van der Ploeg S, Anderson SJ, Kubiszewski I, Farber S, Turner RK (2014) Changes in the global value of ecosystem services. Glob Environ Change 26:152–158

    Google Scholar 

  • Cunning R, Silverstein RN, Baker AC (2015) Investigating the causes and consequences of symbiont shuffling in a multi-partner reef coral symbiosis under environmental change. Proc R Soc B 282:20141725. https://doi.org/10.1098/rspb.2014.1725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol R 76:229–261

    CAS  Google Scholar 

  • De Groot R, Brander L, Van Der Ploeg S, Costanza R, Bernard F, Braat L, Christie M, Crossman N, Ghermandi A, Hein L, Hussain S, Kumar P, McVittie A, Portela R, Rodriguez LC, ten Brink P, van Beukering P (2012) Global estimates of the value of ecosystems and their services in monetary units. Ecosyst Serv 1:50–61

    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. PNAS 109:17995–17999

    PubMed  PubMed Central  Google Scholar 

  • DeBoer TS, Baker AC, Erdmann MV, Ambariyanto A, Jones PR, Barber PH (2012) Patterns of Symbiodinidium distribution in three giant clam species across the biodiverse Bird’s head region of Indonesia. Mar Ecol Prog Ser 444:117–132

    CAS  Google Scholar 

  • DeSalvo MK, Estrada A, Sunagawa S, Medina M (2012) Transcriptomic responses to darkness stress point to common coral bleaching mechanisms. Coral Reefs 31:215–228. https://doi.org/10.1007/s00338-011-0833-834

    Article  Google Scholar 

  • Douglas AE (2003) Coral bleaching–how and why? Mar Pollut Bull 46:385–392

    CAS  PubMed  Google Scholar 

  • Eakin CM, Morgan JA, Heron SF, Smith TB, Liu G, Alvarez-Filip L, Baca B, Bartels E, Bastidas C, Bouchon C, Brandt M et al (2010) Caribbean corals in crisis: record thermal stress, bleaching, and mortality in 2005. PLoS ONE 5:e13969. https://doi.org/10.1371/journal.pone.0013969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fankboner PV (1971) Intracellular digestion of symbiotic zooxanthellae by host amoebocytes in giant clams (Bivalvia: Tridacnidae), with a note on nutritional role of hypertrophied siphonal epidermis. Biol Bull 141:222–234

    Google Scholar 

  • Fitt WK, Fisher CR, Trench RK (1986) Contribution of the symbiotic dinoflagellate Symbiodinium microadriaticum to the nutrition, growth and survival of larval and juvenile tridacnid clams. Aquaculture 55:5–22

    Google Scholar 

  • Ghoshal A, Eck E, Gordon M, Morse DE (2016) Wavelength-specific forward scattering of light by Bragg-reflective iridocytes in giant clams. J R Soc Interface 13:20160285. https://doi.org/10.1098/rsif.2016.0285

    Article  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Griffiths DJ, Winsor H, Luongvan T (1992) Iridophores in the mantle of giant clams. Aus J Zool 40:319–326

    Google Scholar 

  • Hatcher BG (1990) Coral reef primary productivity: a hierarchy of pattern and process. Trends Ecol Evol 5:149–155

    CAS  PubMed  Google Scholar 

  • Hiong KC, Cao-Pham AH, Choo CYL, Boo MV, Wong WP, Chew SF, Ip YK (2017a) Light-dependent expression of a Na+/H+ exchanger 3-like transporter in the ctenidium of the giant clam, Tridacna squamosa, can be related to increased H+ excretion during light-enhanced calcification. Physiol Rep 5:e13209. https://doi.org/10.14814/phy2.13209

  • Hiong KC, Choo CYL, Boo MV, Ching B, Wong WP, Chew SF, Ip YK (2017b) A light-dependent ammonia-assimilating mechanism in the ctenidia of a giant clam. Coral Reefs 36:311–323

    Google Scholar 

  • Hoegh-Guldberg O, Smith GJ (1989) The effect of sudden changes in temperature, light and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata Esper and Seriatopora hystrix Dana. J Exp Mar Biol Ecol 129:279–303

    Google Scholar 

  • Holt AL, Vahidinia S, Gagnon YL, Morse DE, Sweeney AM (2014) Photosymbiotic giant clams are transformers of solar flux. J R Soc Interface 11:20140678. https://doi.org/10.1098/rsif.2014.0678

    Article  PubMed  PubMed Central  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 J-PA, 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 359:80–83

    CAS  PubMed  Google Scholar 

  • Ip YK, Boo MV, Poo JST, Wong WP, Chew SF (2021) Sodium-dependent phosphate transporter protein 1 is involved in the active uptake of inorganic phosphate in nephrocytes of the kidney and the translocation of Pi into the tubular epithelial cells in the outer mantle of the giant clam, Tridacna squamosa. Front Mar Sci 8:655714. https://doi.org/10.3389/fmars.2021.655714

    Article  Google Scholar 

  • Ip YK, Chew SF (2021) Light-Dependent phenomena and related molecular mechanisms in giant clam-dinoflagellate associations: A review. Front Mar Sci 8:627722. https://doi.org/10.3389/fmars.2021.627722

    Article  Google Scholar 

  • Ip YK, Ching B, Hiong KC, Choo CYL, Boo MV, Wong WP, Chew SF (2015) Light induces changes in activities of Na+/K+-ATPase, H+/K+-ATPase and glutamine synthetase in tissues involved directly or indirectly in light-enhanced calcification in the giant clam, Tridacna squamosa. Front Physiol 6:68. https://doi.org/10.3389/fphys.2015.00068

    Article  PubMed  PubMed Central  Google Scholar 

  • Ip YK, Hiong KC, Lim LJY, Choo CYL, Boo MV, Wong WP, Neo ML, Chew SF (2018) Molecular characterization, light-dependent expression, and cellular localization of a host vacuolar-type H+-ATPase (VHA) subunit A in the giant clam, Tridacna squamosa, indicate the involvement of the host VHA in the uptake of inorganic carbon and its supply to the symbiotic zooxanthellae. Gene 659:137–148

    CAS  PubMed  Google Scholar 

  • Ip YK, Hiong KC, Teng JHQ, Boo MV, Choo CYL, Wong WP, Chew SF (2020) The fluted giant clam (Tridacna squamosa) increases nitrate absorption and upregulates the expression of a homolog of SIALIN (H+:2NO3− cotransporter) in the ctenidium during light exposure. Coral Reefs 39:451–465. https://doi.org/10.1007/s00338-020-01907-9

    Article  Google Scholar 

  • Ip YK, Koh CZY, Hiong KC, Choo CYL, Boo MV, Wong WP, Neo ML, Chew SF (2017) Carbonic anhydrase 2-like in the giant clam, Tridacna squamosa: characterization, localization, response to light, and possible role in the transport of inorganic carbon from the host to its symbionts. Physiol Rep 5:e13494. http://doi.org/https://doi.org/10.14814/phy2.13494

  • Jantzen C, Wild C, El-Zibdah M, Roa-Quiaoit HA, Haacke C, Richter C (2008) Photosynthetic performance of giant clams, Tridacna maxima and T. squamosa. Red Sea Mar Biol 155:211–221

    Google Scholar 

  • Jeffery 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

    Google Scholar 

  • Jeffrey SW, Sielicki M, Haxo FT (1975) Chloroplast pigment patterns in dinoflagellates. J Phycol 11:374–384

    CAS  Google Scholar 

  • Jeong HJ, Yoo YD, Kang NS, Lim AS, Seong KA, Lee SY, Lee MJ, Lee KH, Kim HS, Shin W, Nam SW, Yih W, Lee K (2012) Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium. PNAS 109:12604–12609

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jones RJ (1997) Changes in zooxanthellar densities and chlorophyll concentrations in corals during and after a bleaching event. Mar Ecol Prog Ser 158:51–59

    Google Scholar 

  • Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation metabolism in zooxanthellae. Plant Cell Environ 21:1219–1230

    CAS  Google Scholar 

  • Kemp DW, Hernandez-Pech X, Iglesias-Prieto R, Fitt WK, Schmidt GW (2014) Community dynamics and physiology of Symbiodinium spp. before, during, and after a coral bleaching event. Limnol Oceanogr 59:788–797

    CAS  Google Scholar 

  • Klumpp DW, Griffiths CL (1994) Contributions of phototrophic and heterotrophic nutrition to the metabolic and growth requirements of four species of giant clam (Tridacnidae). Mar Ecol Prog Ser 115:103–115

    Google Scholar 

  • Knowlton N, Brainard RE, Fisher R, Moews M, Plaisance L, Caley MJ (2010) Coral reef biodiversity. In: Life in the World’s Oceans: Diversity, Distribution, and Abundance, AD McIntyre (ed.), Blackwell Publishing, Oxford, UK, pp. 65–77

  • Koh CZY, Hiong KC, Choo CYL, Boo MV, Wong WP, Chew SF, Neo ML, Ip YK (2018) Molecular characterization of a dual domain carbonic anhydrase from the ctenidium of the giant clam, Tridacna squamosa, and its expression levels after light exposure, cellular localization, and possible role in the uptake of exogenous inorganic carbon. Front Physiol 9:281. https://doi.org/10.3389/fphys.2018.00281

    Article  PubMed  PubMed Central  Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349. https://doi.org/10.1146/annurev.pp.42.060191.001525

    Article  CAS  Google Scholar 

  • Kushmaro A, Loya Y, Fine M, Rosenberg E (1996) Bacterial infection and coral bleaching. Nature 380:396. https://doi.org/10.1038/380396a0

    Article  CAS  Google Scholar 

  • Leder JJ, Szamnt AM, Swart PK (1991) The effect of prolonged “bleaching” on skeletal banding and stable isotopic composition in Montastrea annularis. Coral Reefs 10:19–27

    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

    CAS  Google Scholar 

  • LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Brown B, Obura DO, Hoegh-Guldberg O, Fitt WK (2010) Long-standing environmental conditions, geographic isolation and host–symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J Biogeogr 37:785–800

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Lesser MP, Shick JM (1989) Effects of irradiance and ultraviolet radiation in photoadaptation in the zooxanthellae of Aiptasia pallida: primary production, photoinhibition, and enzymic defences against oxygen toxicity. Mar Biol 102:243–255

    Google Scholar 

  • Lesser MP, Stochaj WR, Tapley DW, Shick JM (1990) Bleaching in coral reef anthozoans: effects of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against oxygen radicals. Coral Reefs 8:225–232

    Google Scholar 

  • Maruyama T, Heslinga GA (1997) Fecal discharge of zooxanthellae in the giant clam Tridacna derasa, with reference to their in situ growth rate. Mar Biol 127:473–477

    Google Scholar 

  • Mayfield AB, Hsiao YY, Chen HK, Chen CS (2014) Rubisco expression in the dinoflagellate Symbiodinium sp. is influenced by both photoperiod and endosymbiotic lifestyle. Mar Biotechnol 16:371–384

    CAS  Google Scholar 

  • Mies M (2019) Evolution, diversity, distribution and the endangered future of the giant clam–Symbiodiniaceae association. Coral Reefs 38:1067–1084

    Google Scholar 

  • Mies M, Dor P, Güth AZ, Sumida PYG (2017) Production in giant clam aquaculture: trends and challenges. Rev Fish Sci Aquac 4:286–296

    Google Scholar 

  • Morishima S-Y, Yamashita H, O-hara S, Nakamura Y, Quek VZ, Yamauchi M, Koike K (2019) Study on expelled but viable zooxanthellae from giant clams, with an emphasis on their potential as subsequent symbiont sources. PLoS ONE 14(7):e0220141. https://doi.org/10.1371/journal.pone.0220141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moya A, Tambutté S, Tambutté E, Zoccola D, Caminiti N, Allemand D (2006) Study of calcification during a daily cycle of the coral Stylophora pistillata: implications for light-enhanced calcification. J Exp Biol 209:3413–3419

    CAS  PubMed  Google Scholar 

  • Mumby PJ, Chisholm JRM, Edwards AJ, Clark CD, Roark EB, Andrefouet S, Jaubert J (2001) Unprecedented bleaching- induced mortality in Porites spp. at Rogiroa Atoll. French Polynesia Mar Biol 139:183–189

    Google Scholar 

  • Muscatine L, McCloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26:601–611

    CAS  Google Scholar 

  • Neo ML, Eckman W, Vicentuan K, Teo SL-M, Todd PA (2015) The ecological significance of giant clams in coral reef ecosystems. Biol Cons 181:111–123

    Google Scholar 

  • Norton JH, Prior HC, Baillie B, Yellowlees D (1995) Atrophy of the zooxanthellal tubular system in bleached giant clams Tridacna gigas. J Invert Pathol 66:307–310

    Google Scholar 

  • Norton JH, Shepherd MA, Long HM, Fitt WK (1992) The zooxanthellal tubular system in the giant clam. Biol Bull 183:503–506

    CAS  PubMed  Google Scholar 

  • Perez S, Weis V (2006) Nitric oxide and cnidarian bleaching: an eviction notice mediates breakdown of a symbiosis. J Exp Biol 209:2804–2810

    CAS  PubMed  Google Scholar 

  • Poo JST, Choo CYL, Hiong KC, Boo MV, Wong WP, Chew SF, Ip YK (2020) Phototrophic potential and form II ribulose-1,5-bisphosphate carboxylase/oxygenase expression in five organs of the fluted giant clam, Tridacna squamosa. Coral Reefs 39:361–374

    Google Scholar 

  • Poo JST, Boo MV, Chew SF, Ip YK (2021) Using form II ribulose-1,5-bisphosphate carboxylase/oxygenase to estimate the phototrophic potentials of Symbiodinium, Cladocopium and Durusdinium in various organs of the fluted giant clam, Tridacna squamosa, and to evaluate their responses to light upon isolation from the host. Coral Reefs. https://doi.org/10.1007/s00338-020-02031-4

    Article  Google Scholar 

  • Rossbach S, Subedi RC, Ng TK, Ooi BS, Duate CM (2020) Iridocytes mediate photonic cooperation between giant clams (Tridacninae) and their photosynthetic symbionts. Front Mar Sci 7:465. https://doi.org/10.3389/fmars.2020.00465

    Article  Google Scholar 

  • Rouzé H, Hédouin L (2018) Bilateral asymmetry in bleaching susceptibility within a giant clam, Tridacna maxima. Coral Reefs 37:825–825

    Google Scholar 

  • Rowan R, Whitney SM, Fowler A, Yellowlees D (1996) Rubisco in marine symbiotic dinoflagellates: form II enzymes in eukaryotic oxygenic phototrophs encoded by a nuclear multigene family. Plant Cell 8:539–553

    CAS  PubMed  PubMed Central  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, Gates RD (2011) Clade D Symbiodinium in scleractinian corals: a “nugget” of hope, a selfish opportunist, an ominous sign, or all of the above? J Mar Biol 2011:730715. https://doi.org/10.1155/2011/730715

    Article  Google Scholar 

  • Stat M, Pochon X, Franklin EC, Bruno JF, Casey KS, Selig ER, Gates RD (2013) The distribution of the thermally tolerant symbiont lineage (Symbiodinium clade D) in corals from Hawaii: correlations with host and the history of ocean thermal stress. Ecol Evol 3:1317–1329

    PubMed  PubMed Central  Google Scholar 

  • Streamer M, McNeil YR, Yellowlees D (1993) Photosynthetic carbon dioxide fixation in zooxanthellae. Mar Biol 115:195–198

    CAS  Google Scholar 

  • Swain TD, Chandler J, Backman V, Marcelino L (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 31:172–183

    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 8:217–222

    Google Scholar 

  • Teh LSX, Poo JST, Boo MV, Chew SF, Ip YK (2021) Using glutamine synthetase 1 to evaluate the symbionts’ potential of ammonia assimilation and their responses to illumination in five organs of the giant clam, Tridacna squamosa. Comp Biochem Physiol A 55:110914. https://doi.org/10.1016/j.cbpa.2021.110914

    Article  CAS  Google Scholar 

  • Tolleter D, Seneca FO, DeNofrio JC, Krediet CJ, Palumbi SR, Pringle JR, Grossman AR (2013) Coral bleaching independent of photosynthetic activity. Curr Biol 23:1782–1786. https://doi.org/10.1016/j.cub.2013.07.041

    Article  CAS  PubMed  Google Scholar 

  • Tonk L, Sampayo EM, Weeks S, Magno-Canto M, Hoegh-Guldberg O (2013) Host-specific interactions with environmental factors shape the distribution of Symbiodinium across the Great Barrier Reef. PLoS ONE 8:e68533. https://doi.org/10.1371/journal.pone.0068533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Umeki M, Yamashita H, Suzuki G, Sato T, Ohara S, Koike K (2020) Fecal pellets of giant clams as a route for transporting Symbiodiniaceae to corals. PLoS ONE 15(12):e0243087. https://doi.org/10.1371/journal.pone.0243087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Woesik R, De Vantier LM, Glazebrook JS (1995) Effects of Cyclone ‘Joy’ on nearshore coral communities of the Great Barrier Reef. Mar Ecol Prog Ser 128:261–270

    Google Scholar 

  • Vicente VP (1990) Response of sponges with autotrophic endosymbionts during the coral-bleaching episode in Puerto Rico. Coral Reefs 8:199–202

    Google Scholar 

  • Wang J-T, Meng P-J, Sampayo EM, Tang S-L, Chen CA (2011) Photosystem II breakdown induced by reactive oxygen species in freshly-isolated Symbiodinium from Montipora (Scleractinia; Acroporidae). Mar Ecol Prog Ser 422:51–62

    CAS  Google Scholar 

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Acknowledgements

This study was supported by the Singapore Ministry of Education through grants to S. F. Chew (NIE AcRF RI3/19CSF) and to Y. K. Ip (R-154-000-A37-114 and R-154-000-B69-114).

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  1. Department of Biological Sciences, National University of Singapore, Kent Ridge, Singapore, 117543, Republic of Singapore

    Yuen K. Ip & Mel V. Boo

  2. Oceanographic Institute, University of São Paulo, Praça do Oceanográfico 191, São Paulo, SP, 05508-120, Brazil

    Miguel Mies

  3. Natural Sciences and Science Education, National Institute of Education, Nanyang Technological University, 1 Nanyang Walk, Singapore, 637616, Republic of Singapore

    Shit F. Chew

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Ip, Y.K., Boo, M.V., Mies, M. et al. The giant clam Tridacna squamosa quickly regenerates iridocytes and restores symbiont quantity and phototrophic potential to above-control levels in the outer mantle after darkness-induced bleaching. Coral Reefs 41, 35–51 (2022). https://doi.org/10.1007/s00338-021-02199-3

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