Skip to main content

Advertisement

SpringerLink
Log in

Evolution, diversity, distribution and the endangered future of the giant clam–Symbiodiniaceae association

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

Abstract

Giant clams are found in a mutualistic association with Symbiodiniaceae dinoflagellates. While clams are economically important for fisheries, Symbiodiniaceae are responsible for most of the primary production in coral reefs. This review addresses key issues regarding the giant clam–Symbiodiniaceae holobiont: diversity and distribution; functional traits; evolution and coevolution; and consequences of climate change. Findings show that holobiont distribution is partitioned by host species and geography. So far, giant clams have been reported in association with only 30 Symbiodiniaceae phylotypes, all within genera Symbiodinium, Cladocopium and Durusdinium. Species and functional diversities are highest in the Coral Triangle. The association evolved in the Eocene–Oligocene transition; there is evidence for coevolution, including host organs developed for housing symbionts, change in host habitat and multiple symbiont phylotypes found exclusively in giant clams. Clam bleaching events have been recorded throughout the Indo-Pacific. These clams may be particularly vulnerable, as they rarely associate with stress-tolerant symbionts and are heavily targeted by fishing. The Great Barrier Reef is particularly at risk, as clams in that area do not associate with thermally tolerant, low-irradiance-adapted and opportunistic symbiont phylotypes. Further reduction in giant clam populations may serve as an important indicator of the increasing decline of coral reef biodiversity.

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

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

    Google Scholar 

  • Ajith Kumar TT, Balasubramanian T (2012) Bleaching of corals in Agatti-Lakshadweep, India: a window review. In: Proceedings of the 12th international coral reef symposium, Cairns, Australia

  • 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 

  • Andréfouët S, Van Wynsberge S, Kabbadj L, Wabnitz CC, Menkes C, Tamata T, Pahuatini M, Tetairekie I, Teaka I, Scha TA, Teaka T, Remoissenet G (2018) Adaptive management for the sustainable exploitation of lagoon resources in remote islands: lessons from a massive El Niño-induced giant clam bleaching event in the Tuamotu atolls (French Polynesia). Environ Cons 45:30–40

    Google Scholar 

  • Baillie BK, Belda-Baillie CA, Maruyama T (2000) Conspecificity and Indo-Pacific distribution of Symbiodinium genotypes (Dinophyceae) from giant clams. J Phycol 36:1153–1161

    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

    Google Scholar 

  • Bellwood DR, Hoey AS, Hughes TP (2012) Human activity selectively impacts the ecosystem roles of parrotfishes on coral reefs. Proc R Soc B 279:1621–1629

    PubMed  Google Scholar 

  • bin Othman AS, Goh GHS, Todd PA (2010) The distribution and status of giant clams (family Tridacnidae)—a short review. Raff Bull Zool 58:103–111

    Google Scholar 

  • Bongaerts P, Sampayo EM, Bridge TCL, Ridgway T, Vermeulen F, Englebert N, Webster JM, Hoegh-Guldberg O (2011) Symbiodinium diversity in mesophotic coral communities on the Great Barrier Reef: a first assessment. Mar Ecol Prog Ser 439:117–126

    Google Scholar 

  • Braley RD (1992) The Giant Clam: A Hatchery and Nursery Culture Manual. Australian Centre for International Agricultural Research, Canberra

    Google Scholar 

  • Brown JH, Muskanofola MR (1985) An investigation of stocks of giant clams (family Tridacnidae) in Java and of their utilization and potential. Aquacult Fish Manage 1:25–39

    Google Scholar 

  • Bruno JF, Siddon CE, Witman JD, Colin PL, Toscano MA (2001) El Niño related coral bleaching in Palau, Western Caroline Islands. Coral Reefs 20:127–136

    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 

  • Cabaitan PC, Gomez ED, Aliño PM (2008) Effects of coral transplantation and giant clam restocking on the structure of fish communities on degraded patch reefs. J Exp Mar Biol Ecol 357:85–98

    Google Scholar 

  • Canapa A, Barucca M, Marinelli A, Olmo E (2001) A molecular phylogeny of Heterodonta (Bivalvia) based on small ribosomal subunit RNA sequences. Mol Phylogenet Evol 21:156–161

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Chavanich S, Viyakarn V, Adams P, Klammer J, Cook N (2012) Reef communities after the 2010 mass coral bleaching at Racha Yai island in the Andaman Sea and Koh Tao in the Gulf of Thailand. Phuket Marine Biology Centre Research Bulletin 71:103–110

    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 

  • Chew SF, Koh CZY, Hiong KC, Choo CYL, Wong WP, Neo ML, Ip YK (2019) Light-enhanced expression of Carbonic Anhydrase 4-like supports shell formation in the fluted giant clam Tridacna squamosa. Gene 683:101–112

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • de Goeij JM, van Oevelen D, Vermeij MJ, Osinga R, Middelburg JJ, de Goeij AF, Admiraal W (2013) Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science 342:108–110

    PubMed  Google Scholar 

  • DeBoer TS, Baker AC, Erdmann MV, Ambariyanto Barber PH (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

    CAS  Google Scholar 

  • Elfwing T, Plantman P, Tedengren M, Wijnbladh E (2001) Responses to temperature, heavy metal and sediment stress by the giant clam Tridacna squamosa. Mar Freshwater Behav Physiol 34:239–248

    CAS  Google Scholar 

  • Estacion JS, Braley RD (1988) Growth and survival of Tridacna gigas juveniles in an intertidal pond. In: Copland JW, Lucas JS (eds) Giant Clams in Asia and the Pacific. ACIAR Monograph Series No. 9, Canberra, pp 191–192

    Google Scholar 

  • Farmer MA, Fitt WK, Trench RK (2001) Morphology of the symbiosis between Corculum cardissa (Mollusca: Bivalvia) and Symbiodinium corculorum (Dinophyceae). Biol Bull 200:336–343

    CAS  PubMed  Google Scholar 

  • Fauvelot C, Andréfouët S, Grulois D, Tiavouane J, Wabnitz CC, Magalon H, Borsa P (2017) Phylogeography of Noah’s giant clam. Mar Biodivers. https://doi.org/10.1007/s12526-017-0794-0

    Article  Google Scholar 

  • Fensome RA, Saldarriaga JF, Taylor FJRM (1999) Dinoflagellate phylogeny revisited: reconciling morphological and molecular based phylogenies. Grana 38:66–80

    Google Scholar 

  • Finney JC, Pettay DT, Sampayo EM, Warner ME, Oxenford HA, LaJeunesse TC (2010) The relative significance of host-habitat, depth, and geography on the ecology, endemism, and speciation of coral endosymbionts in the genus Symbiodinium. Microb Ecol 60:250–263

    PubMed  Google Scholar 

  • Fitt WK, Fisher CR, Trench RK (1984) Larval biology of tridacnid clams. Aquaculture 39:181–195

    Google Scholar 

  • Fitt WK, Trench RK (1981) Spawning, development, and acquisition of zooxanthellae by Tridacna squamosa (Mollusca, Bivalvia). Biol Bull 161:213–235

    Google Scholar 

  • Frieler K, Meinshausen M, Golly A, Mengel M, Lebek K, Donner SD, Hoegh-Guldberg O (2013) Limiting global warming to 2°C is unlikely to save most coral reefs. Nat Clim Change 3:165–170

    Google Scholar 

  • Gillett R (2016) Fisheries in the Economies of Pacific Island Countries and Territories. Secretariat of the Pacific Community, Noumea, New Caledonia

    Google Scholar 

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

    Google Scholar 

  • Gomez ED, Mingoa-Licuanan SS (1998) Mortalities of giant clams associated with unusually high temperatures and coral bleaching. Reef Encounter 24:23

    Google Scholar 

  • Gomez ED, Mingoa-Licuanan SS (2006) Achievements and lessons learned in restocking giant clams in Philippines. Fisheries Research 80:46–52

    Google Scholar 

  • Harzhauser M, Mandic O, Piller WE, Reuter M, Kroh A (2008) Tracing back the origin of the Indo-Pacific mollusc fauna: basal Tridacninae from the Oligocene and Miocene of the Sultanate of Oman. Palaeontology 51:199–213

    Google Scholar 

  • Hennige SJ, Suggett DJ, Warner ME, McDougall KE, Smith DJ (2009) Photobiology of Symbiodinium revisited: bio-physical and bio-optical signatures. Coral Reefs 28:179–195

    Google Scholar 

  • Herrera ND, ter Poorten JJ, Bieler R, Mikkelsen PM, Strong EE, Jablonski D, Steppan SJ (2015) Molecular phylogenetics and historical biogeography amid shifting continents in the cockles and giant clams (Bivalvia: Cardiidae). Mol Phylogenet Evol 93:94–106

    PubMed  Google Scholar 

  • Heslinga GA, Perron FE, Orak O (1984) Mass culture of giant clams (F. Tridacnidae) in Palau. Aquaculture 39:197–215

    Google Scholar 

  • Hirose E, Iwai K, Maruyama T (2006) Establishment of the photosymbiosis in the early ontogeny of three giant clams. Mar Biol 148:551–558

    Google Scholar 

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

    Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RD, Greenfield P, Gomez ED, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    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 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 

  • Hui M, Kochzius M, Leese F (2012) Isolation and characterisation of nine microsatellite markers in the boring giant clam (Tridacna crocea) and cross-amplification in five other tridacnid species. Mar Biodivers 42:285–287

    Google Scholar 

  • Hume BCC, Voolstra CR, Arif C, D’Angelo C, Burt JA, Eyal G, Loya Y, Wiedenmann J (2016) Ancestral genetic diversity associated with the rapid spread of stress-tolerant coralsymbionts in response to Holocene climate change. Proc Natl Acad Sci USA 113:4416–4421

    CAS  PubMed  Google Scholar 

  • Hume BCC, Ziegler M, Poulain J, Pochon X, Romac S, Boissin E, de Vargas C, Planes S, Wincker P, Voolstra CR (2018) An improved primer set and amplification protocol with increased specificity and sensitivity targeting the Symbiodinium ITS2 region. PeerJ 6:e4816

    PubMed  PubMed Central  Google Scholar 

  • Iglesias-Prieto R, Trench RK (1997) Photoadaptation, photoacclimation and niche diversification in invertebrate-dinoflagellate symbioses. In: Proceedings of the 8th international coral reef symposium

  • Ikeda S, Yamashita H, Kondo S, Inoue K, Morishima S, Koike K (2017) Zooxanthellal genetic varieties in giant clams are partially determined by species-intrinsic and growth-related characteristics. PLoS ONE 12:e0172285

    PubMed  PubMed Central  Google Scholar 

  • Ishikura M, Adachi K, Maruyama T (1999) Zooxanthellae release glucose in the tissue of a giant clam, Tridacna crocea. Mar Biol 133:665–673

    CAS  Google Scholar 

  • Ishikura M, Hagiwara K, Takishita K, Haga M, Iwai K, Maruyama T (2004) Isolation of new Symbiodinium strains from tridacnid giant clam (Tridacna crocea) and sea slug (Pteraeolidia ianthina) using culture medium containing giant clam tissue homogenate. Mar Biotechnol 6:378–385

    CAS  PubMed  Google Scholar 

  • Ishikura M, Kato C, Maruyama T (1997) UV-absorbing substances in zooxanthellate and azooxanthellate clams. Mar Biol 128:649–655

    CAS  Google Scholar 

  • IUCN (2016) The IUCN red list of threatened species. Version 2016-2 [Online]. www.iucnredlist.org

  • 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 

  • Junchompoo C, Sinrapasan N, Penpian C, Patsorn P (2013) Changing seawater temperature effects on giant clams belaching, Mannai Island, Rayong Province, Thailand. In: Proceedings of the design symposium on conservation of ecosystem

  • Karako S, Stambler N, Dubinsky Z (2002) The taxonomy and evolution of the zooxanthellae-coral symbiosis. In: Seckbach J (ed) Symbiosis: Mechanisms and Model Systems. Kluwer Academic Publishers, The Netherlands, pp 539–557

    Google Scholar 

  • Keyse J, Treml EA, Huelsken T, Barber PH, DeBoer TS, Kochzius M, Nuryanto A, Gardner JPA, Liu L-L, Penny S, Riginos C (2018) Historical divergences associated with intermittent land bridges overshadow isolation by larval dispersal in co-distributed species of Tridacna giant clams. J Biogeogr. https://doi.org/10.1111/jbi.13163

    Article  Google Scholar 

  • Kiessling W, Baron-Szabo RC (2004) Extinction and recovery patterns of scleractinian corals at the Cretaceous-Tertiary boundary. Palaeogeogr Palaeoclimatol Palaeoecol 214:195–223

    Google Scholar 

  • Kirkendale L, Paulay G (2017) Part N, revised, volume 1, chapter 9: photosymbiosis in Bivalvia. Treat Online 89:1–39

    Google Scholar 

  • Klumpp DW, Bayne BL, Hawkins AJS (1992) Nutrition of the giant clam Tridacna gigas (L.). I. Contribution of filter feeding and photosynthates to respirations and growth. J Exp Mar Biol Ecol 155:105–122

    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 

  • Krishnan P, Dam Roy D, George G, Srivastava RC, Anand A, Murugesan S, Kaliyamoorthy M, Vikas N, Soundararajan R (2011) Elevated sea surface temperature during May 2010 induces mass bleaching of corals in the Andaman. Curr Sci 100:111–117

    Google Scholar 

  • LaJeunesse TC (2001) Investigating the biodivesrity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a “species” level marker. J Phycol 37:866–880

    CAS  Google Scholar 

  • LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400

    Google Scholar 

  • LaJeunesse TC (2005) “Species” radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol 22:570–581

    CAS  PubMed  Google Scholar 

  • LaJeunesse TC, Bhagooli R, Hidaka M, deVantier L, Done T, Schmidt GW, Fitt WK, Hoegh-Guldberg O (2004) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar Ecol Prog Ser 284:147–161

    Google Scholar 

  • LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28:1–11

    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 therelative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J Biogeogr 37:785–800

    Google Scholar 

  • LaJeunesse TC, Wham D, Tye Pettay D, Parkinson JE, Keshavmurthy S, Chen CA (2014) Ecologically differentiated stress-tolerant endosymbionts in the dinoflagellate genus Symbiodinium (Dinophyceae) Clade D are different species. Phycologia 53:305–319

    Google Scholar 

  • Lee SY, Jeong HJ, Kang NS, Jang TY, Jang SH, LaJeunesse TC (2015) Symbiodinium tridacnidorum sp. nov., a dinoflagellate common to Indo-Pacific giant clams, and a revised morphological description of Symbiodinium microadriaticum Freudenthal, emended Trench & Blank. Eur J Phycol 50:155–172

    Google Scholar 

  • Leggat W, Buck BH, Grice AM, 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 

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

    CAS  PubMed  Google Scholar 

  • Lim SSQ, Huang D, Soong K, Neo ML (2019) Diversity of endosymbiotic Symbiodiniaceae in giant clams at Dongsha Atoll, northern South China Sea. Symbiosis. https://doi.org/10.1007/s13199-019-00615-5

    Article  Google Scholar 

  • Lucas JS (1994) The biology, exploitation, and mariculture of giant clams (Tridacnidae). Rev Fish Sci 2:181–223

    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 

  • Mekawy MS, Madkour HA (2012) Studies on the Indo-Pacific Tridacnidae (Tridacna maxima) from the Northern Red Sea, Egypt. International Journal of Geosciences 3:1089–1095

    Google Scholar 

  • Mieog JC, Olsen JL, Berkelmans R, Bleuler-Martinez SA, Willis BL, van Oppen MJH (2009) The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS ONE 4:e6364

    PubMed  PubMed Central  Google Scholar 

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

    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 36:1319–1328

    Google Scholar 

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

    Google Scholar 

  • Mies M, Güth AZ, Castro CB, Pires DO, Calderon EN, Pompeu M, Sumida PYG (2018) Bleaching in reef invertebrate larvae associated with Symbiodinium strains within clades A-F. Mar Biol 165:6

    Google Scholar 

  • Mies M, Scozzafave MS, Braga F, Sumida PYG (2017c) Giant clams. In: Calado R, Olivotto I, Planas M, Holt GJ (eds) Marine Ornamental Species Aquaculture. Wiley-Blackwell Publishing, Oxford, UK, pp 510–535

    Google Scholar 

  • Mies M, Sumida PYG, Rädecker N, Voolstra CR (2017d) Marine invertebrate larvae associated with Symbiodinium: a mutualism from the start? Front Ecol Evol 5:56

    Google Scholar 

  • Mies M, Van Sluys M-A, Metcalfe CJ, Sumida PYG (2017e) Molecular evidence of symbiotic activity between Symbiodinium and Tridacna maxima larvae. Symbiosis 72:13–22

    CAS  Google Scholar 

  • Mies M, Voolstra CR, Castro CB, Pires DO, Calderon EN, Sumida PYG (2017f) Expression of a symbiosis-specific gene in Symbiodinium type A1 associated with coral, nudibranch and giant clam larvae. R Soc Open Sci 4:170253

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Moldowan JM, Dahl J, Jacobson JR, Huizinga BJ, Fago FJ, Shetty R, Watt DS, Peters KE (1996) Chemostratigraphic reconstruction of biofacies: molecular evidence linking cyst-forming dinoflagellates with pre-Triassic ancestors. Geology 24:159–162

    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 

  • Neo ML, Wabnitz CC, Braley RD, Heslinga GA, Fauvelot C, Van Wynsberge S, Andréfouët S, Waters C, Tan AS, Gomez ED, Costello MJ, Todd PA (2017) Giant clams (Bivalvia: Cardiidae: Tridacninae): a comprehensive update of species and their distribution, current threats and conservation status. Oceanography and Marine Biology 55:87–388

    Google Scholar 

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

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Pappas M (2017) The stability of the giant clam holobiont over time and during bleaching stress. Master Thesis, King Abdullah University of Science and Technology, Saudi Arabia

  • Plantman P, Wijnbladh X, Tedengren M (2000) Abundance, size and depth distribution of the giant clams, Tridacna squamosa and T. crocea in the Gulf of Thailand. In: Proceedings of the 5th Asian fishery forum

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

    CAS  PubMed  Google Scholar 

  • Pochon X, LaJeunesse TC, Pawlowski J (2004) Biogeographic partitioning and host specialization among foraminiferan dinoflagellate symbionts (Symbiodinium; Dinophyta). Mar Biol 146:17–27

    Google Scholar 

  • Pochon X, Montoya-Burgos JI, Stadelmann B, Pawlowski J (2006) Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol Phylogenet Evol 38:20–30

    CAS  PubMed  Google Scholar 

  • Pochon X, Pawlowski J (2006) Evolution of the soritids-Symbiodinium symbiosis. Symbiosis 42:77–88

    Google Scholar 

  • Pochon X, Putnam HM, Gates RD (2014) Multi-gene analysis of Symbiodinium dinoflagellates: a perspective on rarity, symbiosis, and evolution. PeerJ 2:e394

    PubMed  PubMed Central  Google Scholar 

  • Richter C, Roa-Quiaoit H, Jantzen C, Al-Zibdah M, Kochzius M (2008) Collapse of a new living species of giant clam in the Red Sea. Curr Biol 18:1349–1354

    CAS  PubMed  Google Scholar 

  • Roberts CM, McClean CJ, Veron JEN, Hawkins JP, Allen GR, McAllister DE, Mittermeier CG, Schueler FW, Spalding M, Wells F, Vynne C, Werner TB (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295:1280–1284

    CAS  PubMed  Google Scholar 

  • Robison JD, Warner ME (2006) Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). J Phycol 42:568–579

    CAS  Google Scholar 

  • Rosewater J (1965) The family Tridacnidae in the Indo-Pacific. Indo-Pacific Mollusca 1:347–396

    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 

  • Rouzé H, Hédouin L (2018) Bilateral asymmetry in bleaching susceptibility within a giant clam, Tridacna maxima. Coral Reefs 37(3):825

    Google Scholar 

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

    CAS  Google Scholar 

  • Rowan R, Powers DA (1992) Ribosomal RNA sequences and the diversity of symbiotic dinoflagellates (zooxanthellae). Proc Natl Acad Sci USA 89:3639–3643

    CAS  PubMed  Google Scholar 

  • Ruscoe EJ (1962) Some records of large Tridacna specimens. Hawaiian Shell News 11:8

    Google Scholar 

  • Sampayo EM, Franceschinis L, Hoegh-Guldberg O, Dove S (2007) Niche partitioning of closely related symbiotic dinoflagellates. Mol Ecol 16:3721–3733

    CAS  PubMed  Google Scholar 

  • Sangmanee K, Sutthacheep M (2010) Bleaching and mortality of giant clams in the Andaman Sea. In: Proceedings of the 36th congress on science and technology of Thailand

  • Santos SR, Taylor DJ, Kinzie RA III, Hidaka M, Sakai K, Coffroth MA (2002) Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences. Mol Phylogenet Evol 23:97–111

    CAS  PubMed  Google Scholar 

  • Schneider JA (1995) Phylogeny of the Cardiidae (Mollusca, Bivalvia): Protocardiinae, Laevicardiinae, Lahilliinae, Tulongocardiinae subfam. and Pleuriocardiinae subfam. Zool Scripta 24:321–346

    Google Scholar 

  • Schneider JA, Foighil DÓ (1999) Phylogeny of giant clams (Cardiidae: Tridacninae) based on partial mitochondrial 16S rDNA gene sequences. Mol Phylogenet Evol 13:59–66

    CAS  PubMed  Google Scholar 

  • Schoenberg DA, Trench RK (1980) Genetic variation in Symbiodinium (= Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. I. Isoenzyme and soluble protein patterns of axenic cultures of Symbiodinium microadriaticum. Proc R Soc B 207:405–427

    CAS  Google Scholar 

  • Siebeck UE, Marshall NJ, Klüter A, Hoegh-Guldberg O (2006) Monitoring coral bleaching using a colour reference card. Coral Reefs 25:453–460

    Google Scholar 

  • Smith EG, Ketchum RN, Burt JA (2017) Host specificity of Symbiodinium variants revealed by an ITS2 metahaplotype approach. ISME J 11:1500–1503

    CAS  PubMed  PubMed Central  Google Scholar 

  • Spencer T, Telek KA, Bradshaw C, Spalding MD (2000) Coral bleaching in the southern Seychelles during the 1997–1998 Indian Ocean Warm event. Marine Poll Bull 40:569–586

    CAS  Google Scholar 

  • Stanley GD (2003) The evolution of modern corals and their early history. Earth Sci Rev 60:195–225

    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 105:9256–9261

    CAS  PubMed  Google Scholar 

  • Suggett DJ, Warner ME, Leggat W (2017) Symbiotic dinoflagellate functional diversity mediates coral survival under ecological crisis. Trends Ecol Evol 32:735–745

    PubMed  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 

  • Takabayashi M, Santos SR, Cook CB (2004) Mitochondrial DNA phylogeny of the symbiotic dinoflagellates (Symbiodinium, Dinophyta). J Phycol 40:160–164

    CAS  Google Scholar 

  • Takishita K, Ishikura M, Koike K, Maruyama T (2003) Comparison of phylogenies based on nuclear-encoded SSU rDNA and plastid-encoded psbA in the symbiotic dinoflagellate genus Symbiodinium. Phycologia 42:469–481

    Google Scholar 

  • Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, Häggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 101:13531–13535

    CAS  PubMed  Google Scholar 

  • Teitelbaum A, Friedman K (2008) Successes and failures in reintroducting giant clams in the Indo-Pacific region. SPC Trochus Information Bulletin 14:19–26

    Google Scholar 

  • Thornhill DJ, Lewis AM, Wham D, LaJeunesse TC (2014) Host-specialist lineages dominate the adaptive radiation of reef coral endosymbionts. Evolution 68:352–367

    CAS  PubMed  Google Scholar 

  • Tisdell C, Thomas WR, Tacconi L, Lucas JS (1993) The cost of production of giant clam seed Tridacna gigas. J World Aquacult Soc 24:352–360

    Google Scholar 

  • Toonen RJ, Nakayama T, Ogawa T, Rossiter A, Delbeek JC (2012) Growth of cultured giant clams (Tridacna spp.) in low pH, high-nutrient seawater: species-specific effects of substrate and supplemental feeding under acidification. J Mar Biol Assoc U. K. 92:731–740

    CAS  Google Scholar 

  • Tun K, Chou LM, Low J, Yeemin T, Phongsuwan N, Setiasih N, Wilson J, Amri AY, Adzis KAA, Lane D, van Bochove J-W, Kluskens B, Long NV, Tuan VS, Gomez ED (2010) A regional overview on the 2010 coral bleaching event in Southeast Asia. In: Kimura T, Tun KC (eds) Status of Coral Reefs in East Asian Seas Region: 2010. Japan Ministry of the Environment, Tokyo, pp 16–27

    Google Scholar 

  • Turner JR, Hardman E, Klaus R, Fagoonee I, Daby D, Bhagooli R, Persands S (2000) The reefs of Mauritius. In: Souter D, Obura D, Linden O (eds) Coral Reef Degradation in the Indian Ocean. Cordio, Stockholm, pp 94–107

    Google Scholar 

  • Ulstrup KE, van Oppen MJH (2003) Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Mol Ecol 12:3477–3484

    CAS  PubMed  Google Scholar 

  • Van Wynsberge S, Andréfouët S (2017) The future of giant clam-dominated lagoon ecosystems facing climate change. Current Climate Change Reports 3:261–270

    Google Scholar 

  • Van Wynsberge S, Andréfouët S, Gaertner-Mazouni N, Wabnitz CCC, Gilbert A, Remoissenet G, Payri C, Fauvelot C (2016) Drivers of density for the exploited giant clam Tridacna maxima: a meta-analysis. Fish and Fisheries 17:567–584

    Google Scholar 

  • Van Wynsberge S, Andréfouët S, Gaertner-Mazouni N, Remoissenet G (2018) Consequences of an uncertain mass mortality regime triggered by climate variability on giant clam population management in the Pacific Ocean. Theor Popul Biol 119:37–47

    PubMed  Google Scholar 

  • Vinoth R, Gopi M, Ajith Kumar TT, Thangaradjou T, Balasubramanian T (2012) Coral reef bleaching at Agatti Island of Lakshadweep Atolls, India. J Ocean U China 11:105–110

    Google Scholar 

  • Watson S-A, Southgate PC, Miller GM, Moorhead JA, Knauer J (2012) Ocean acidification and warming reduce juvenile survival of the fluted giant clam, Tridacna squamosa. Molluscan Res 32:177–180

    Google Scholar 

  • Weber MX (2009) The biogeography and evolution of Symbiodinium in giant clams (Tridacnidae). Ph.D. Dissertation, University of California, Berkeley

  • Wenger A, Fabricius KE, Jones GP, Brodie JE (2015) Effects of sedimentation, eutrophication and chemical pollution on coral reef fishes. In: Mora C (ed) Ecology of Fishes on Coral Reefs. Cambridge University Press, Cambridge, UK, pp 145–153

    Google Scholar 

  • Wietheger A, Starzak DE, Gould KS, Davy SK (2018) Differential ROS generation in response to stress in Symbiodinium spp. Biol Bull 234:11–21

    CAS  PubMed  Google Scholar 

  • White M (2019) Initial assessment of a new coral bleaching event at Tongareva Atoll in the northern Cook Islands. Hakono Hararanga Incorporated report

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

    CAS  Google Scholar 

Download references

Acknowledgements

I would like to thank the anonymous reviewers, Linda Waters, Maurício Shimabukuro, Arthur Güth and Paulo Sumida for their comments on the manuscript, and Juliana Ali and Arthur Güth for the illustrations.

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

    Miguel Mies

Authors
  1. Miguel Mies
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MM compiled and analyzed the data and wrote the manuscript.

Corresponding author

Correspondence to Miguel Mies.

Ethics declarations

Conflict of interest

The author declares that he have no conflict of interest.

Additional information

Publisher's Note

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

Topic editor Simon Davy.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mies, M. Evolution, diversity, distribution and the endangered future of the giant clam–Symbiodiniaceae association. Coral Reefs 38, 1067–1084 (2019). https://doi.org/10.1007/s00338-019-01857-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-019-01857-x

Keywords

Search

Navigation