Advertisement

Climate Change and Bivalve Mass Mortality in Temperate Regions

  • Tan Kar Soon
  • Huaiping ZhengEmail author
Chapter
Part of the Reviews of Environmental Contamination and Toxicology book series (RECT, volume 251)

Abstract

One of the fastest-growing global food sectors is the bivalve aquaculture industry. Bivalves particularly oysters, mussels and clams are important sources of animal protein (Tan and Ransangan 2016a, b). Bivalve aquaculture represents 14–16% of the average per capita animal protein for 1.5 billion people and supports over 200,000 livelihoods, mostly in developing countries (FAO 2018). Most of the bivalves produced around the world (89%) are from aquaculture (FAO 2016). To date, mollusc aquaculture have accounted for 21.42% (17.14 million tonnes) of the total aquaculture production, with Asia being the largest contributor (92.27%) (FAO 2018).

Keywords

Bivalve mass mortality Climate change Warming Ocean acidification 

Abbreviations

OA

Ocean acidification

HABs

Harmful algal blooms

ROD

Roseovarius oyster disease

IPCC

Intergovernmental panel on climate change

USA

United States of America

UK

United Kingdom

OH

Hydroxide

CO32–

Carbonate

Notes

Acknowledgements

The present study was financially supported by the National Natural Science Foundation of China (31872563), National Key R&D Program of China (2018YFD0901400), China Modern Agro-industry Technology Research System (CARS-49) and Department of Education of Guangdong Province (2017KCXTD014), China. We are very grateful to Dr. Jude Juventus Aweya (Department of Biology, Shantou University) for proofreading and English editing.

References

  1. Barton AD, Irwin AJ, Finkel ZV, Stock CA (2016) Anthropogenic climate change drives shift and shuffle in North Atlantic phytoplankton communities. Proc Natl Acad Sci U S A 113(11):2964–2969Google Scholar
  2. Basti L, Segawa S (2010) Mortalities of the short-neck clam Ruditapes philippinarum induced by the toxic dinoflagellate Heterocapsa circularisquama. Fish Sci 76:625–631Google Scholar
  3. Basti L, Nagai K, Shimasaki Y, Oshima Y, Honjo T, Segawa S (2009) Effects of the toxic dinoflagellate Heterocapsa circularisquama on the valve movement behaviour of the Manila clam Ruditapes philippinarum. Aquaculture 291:41–47Google Scholar
  4. Boardman CL, Maloy AP, Boettcher KJ (2008) Localization of the bacterial agent of juvenile oyster disease (Roseovarius crassostreae) within affected eastern oysters (Crassostrea virginica). J Invertebr Pathol 97:150–158Google Scholar
  5. Boettcher KJ, Geaghan KK, Maloy AP, Barber BJ (2005) Roseovarius crassostreae sp. nov., a member of the Roseobacter clade and the apparent cause of juvenile oyster disease (JOD) in cultured Eastern oysters. Int J Syst Evol Microbiol 55:1531–1537Google Scholar
  6. Bressan M, Chinellato A, Munari M, Matozzo V, Manci A, Marceta T, Finos L, Moro I, Pastore P, Badocco D, Marin MG (2014) Does seawater acidification affect survival, growth and shell integrity in bivalve juveniles? Mar Environ Res 99:136–148Google Scholar
  7. Bricelj VM, Kuenstner SH (1989) Effects of the “Brown tide” on the feeding physiology and growth of bay scallops and mussels. In: Cosper EM, Bricelj VM, Carpenter EJ (eds) Novel phytoplankton blooms. Coastal and estuarine studies (formerly Lecture Notes on Coastal and Estuarine Studies), vol 35. Springer, BerlinGoogle Scholar
  8. Bricelj VM, MacQuarrie SP (2007) Effects of brown tide (Aureococcus anophagefferens) on hard clam Mercenaria mercenaria larvae and implications for benthic recruitment. Mar Ecol Prog Ser 331:147–159Google Scholar
  9. Bricelj VM, Epp J, Malouf R, E. (1987) Intraspecific variation in reproductive and somatic growth cycles of bay scallops Argopecten irradians. Mar Ecol Prog Ser 36:123–137Google Scholar
  10. Bricelj VM, Ford SE, Borrero FJ, Perkins FO, Rivara G, Hillman RE, Elston RA, Chang J (1992) Unexplained mortalities of hatchery-reared, juvenile oysters, Crassostrea virginica (Gmelin). J Shellfish Res 11:331–347Google Scholar
  11. Bricelj VM, MacQuarrie SP, Schaffner RA (2001) Differential effects of Aureococcus anophagefferens isolates ("brown tide") in unialgal and mixed suspensions on bivalve feeding. Mar Biol 139:605–615Google Scholar
  12. Bushek D, Ford SE, Burt I (2012) Long-term patterns of an estuarine pathogen along a salinity gradient. J Mar Res 70:225–251Google Scholar
  13. Byrne RH (2002) Inorganic speciation of dissolved elements in seawater: the influence of pH on concentration ratios. Geochem Trans 3:11–16Google Scholar
  14. Caceres-Martinez J, Madero-Lopez LH, Padilla-Lardizabal G, Vasquez-Yeomans R (2016) Epizootiology of Perkinsus marinus, parasite of the pleasure oyster Crassostrea corteziensis, in the Pacific coast of Mexico. J Invertebr Pathol 139:12–18Google Scholar
  15. Callaway R, Burdon D, Deasey A, Mazik K, Elliott M (2013) The riddle of the sands: population dynamics provides clues to causes of high cockle mortality. J Appl Ecol 50:1050–1059Google Scholar
  16. Chen M, Yang H, Delaporte M, Zhao S (2007) Immune condition of Chlamys farreri in response to acute temperature challenge. Aquaculture 271:479–487Google Scholar
  17. Cheney DP, MacDonald BF, Elston RA (2000) Summer mortality of Pacific oysters Crassostrea gigas (Thunberg): initial findings on multiple environmental stressors in Puget Sound, Washington, 1998. J Shellfish Res 19(1):353–359Google Scholar
  18. Comps M, Cochennec N (1993) A herpes-like virus from the European oyster Ostrea edulis L. J Invertebr Pathol 62:201–203Google Scholar
  19. Cook T, Folli M, Klinck J, Ford S, Miller J (1998) The relationship between increasing sea-surface temperature and the northward spread of Perkinsus marinus (Dermo) disease epizootics in oysters. Estuar Coast Shelf Sci 46:587–597Google Scholar
  20. Da Silva PM, Renault T, Fuentes J, Villalba A (2008) Herpesvirus infection in European flat oysters Ostrea edulis obtained from brood stocks of various geographic origins and grown in Galicia (NW Spain). Dis Aquat Organ 78:181–188Google Scholar
  21. Davis CV, Barber BJ (1994) Size-dependent mortality in hatchery-reared populations of oysters, Crassostrea virginica, Gmelin 1791, affected by juvenile oyster disease. J Shellfish Res 13:137–142Google Scholar
  22. Defeo O, Castrejón M, Ortega L, Kuhn AM, Gutiérrez NL, Castilla JC (2013) Impacts of climate variability on Latin American small-scale fisheries. Ecol Soc 18:30Google Scholar
  23. Degerman R, Dinasquet J, Riemann L, de Luna SS, Anderson A (2013) Effect of resource availability on bacterial community responses to increased temperature. Aquat Microb Ecol 68:131–142Google Scholar
  24. Degremont L, Bedier E, Soletchnik P, Ropert M, Huvet A, Moal J, Samain JF, Boudry P (2005) Relative importance of family, site, and field placement timing on survival, growth, and yield of hatchery-produced Pacific oyster spat (Crassostrea gigas). Aquaculture 249:213–229Google Scholar
  25. Deser C, Phillips AS, Alexander MA (2010) Twentieth century tropical sea surface temperature trends revisited. Geophys Res Lett 37Google Scholar
  26. Deslou-Paoli JM, Herl M, Berthome JP, Razel D, Garnier J (1982) Reproduction naturelle de Crassostrea gigas Thunberg dans le basin de Marennes-Oleron en 1979 et 1981: aspects biochimiques et energetiques. Rev Trav Inst Pech Marit 45:319–327Google Scholar
  27. Draper C, Gainey L, Shumway S, Shapiro L (1990) Effects of Aureococcus anophagefferens (“brown tide”) on the lateral cilia of 5 species of bivalve molluscs. In: Graneli E et al (eds) Toxic marine phytoplankton. Proceedings of the 4th international conference. Elsevier, New York, pp 128–131Google Scholar
  28. Enriquez-Espinoza TL, Grijalva-Chon JM, Castro-Longoria R, Ramos-Paredes J (2010) Perkinsus marinus in Crassostrea gigas in the Gulf of California. Dis Aquat Organ 89:269–273Google Scholar
  29. FAO (2016) The State of World Fisheries and Aquaculture 2016. Contributing to food security and nutrition for all. RomeGoogle Scholar
  30. FAO (2018) The State of World Fisheries and Aquaculture 2018: meeting the sustainable developing goals. Rome. Licence: CC BY-NC-SA 3.0 IGOGoogle Scholar
  31. Farley CA, Banfield WG, Kasnic JRG, Foster WS (1972) Oyster herpes-type virus. Science 178:759–760Google Scholar
  32. Feely RA, Sabine CL, Lee K, Berelson W, Kleypas J, Fabry VJ (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305:362–366Google Scholar
  33. Feely RA, Doney SC, Cooley SR (2009) Ocean acidification: present conditions and future changes in a high-CO2 world. Oceanography 22:36–47Google Scholar
  34. Filgueira R, Guyondet T, Comeau LA, Tremblay R (2016) Bivalve aquaculture-environment interactions in the context of climate change. Glob Chang Biol 22(12):3901–3913Google Scholar
  35. Fiori S, Cazzaniga N (1999) Mass mortality of the yellow clam, Mesodesma mactroides (Bivalvia, Mesodesmatidae) in Monte Hermoso Beach, Argentina. Biol Conserv 89:305–309Google Scholar
  36. Ford SE (1996) Range extension by the oyster parasite Perkinsus marinus into the northern US: response to climate change? J Shellfish Res 15:45–56Google Scholar
  37. Ford SE (2011) Dermo disease of oysters caused by Perkinsus marinus. In: Ford SE (ed) ICES identification leaflets for diseases and parasites of fish and shellfish. ICES, CopenhagenGoogle Scholar
  38. Ford SE, Borrero FJ (2001) Epizootiology and pathology of juvenile oyster disease in the Eastern oyster, Crassostrea virginica. J Invertebr Pathol 78(3):141–154Google Scholar
  39. Gagnaire B, Frouin H, Moreau K, Thomas-Guyon H, Renault T (2006) Effects of temperature and salinity on haemocyte activities of the Pacific oyster, Crassostrea gigas (Thunberg). Fish Shellfish Immunol 20:536–547Google Scholar
  40. Gainey LF, Shumway SE (1991) The physiological effect of Aureococcus anophagefferens (‘brown tide’) on the lateral cilia of bivalve mollusks. Biol Bull 181:298–306Google Scholar
  41. Garnier M, Labreuche Y, Garcia C, Robert M, Nicolas JL (2007) Evidence for the involvement of pathogenic bacteria in summer mortalities of the Pacific oyster Crassostrea gigas. Microb Ecol 53:187–196Google Scholar
  42. Gattuso JP, Hansson L (eds) (2011) Ocean acidification. Oxford University Press, OxfordGoogle Scholar
  43. Gazeau F, Quiblier C, Jansen JM, Gattuso JP, Middelburg JJ Heip CHR (2007) Impact of elevated CO2 on shellfish calcification. Geophys Res Lett 34Google Scholar
  44. Gazeau F, Alliouane S, Bock C, Bramanti L, Gentille M, Hirse T, Lopez M, Correa H-O, Pörtner HO, Ziveri P (2014) Impact of ocean acidification and warming on the Mediterranean mussel (Mytilus galloprovincialis). Front Mar Sci 1:62Google Scholar
  45. Gobler CJ, Lonsdale DJ, Boyer GL (2005) A synthesis and review of causes and impact of harmful brown tide blooms caused by the alga, Aureococcus anophagefferens. Estuaries 28:726–749Google Scholar
  46. Gobler CJ, Doherty OM, Hattenrath-Lehmann TK, Griffith AW, Kang Y, Litaker RW (2017) Ocean warming since 1982 has expanded the niche of toxic algal blooms in the North Atlantic and North Pacific oceans. Proc Natl Acad Sci U S A 114(19):4975–4980Google Scholar
  47. Gonzalez R, Perez Camacho A (1984) El berberecho, Cerastoderma edule (L.) de Carril (Ria de Arosa) II: Reclutamiento, crecimiento, mortalidad natural y produccion. Actas IV Simposio Iberico do Estudos Do Benthos Marinho 2:223–244Google Scholar
  48. Goulletquer P, Soletchnick P, Le Moine O, Razet D, Geairon P, Faury N, Taillade S (1998) Summer mortality of the Pacific cupped oyster Crassostrea gigas in the Bay of Marennes-Oléron (France). Ices Statutory Meeting, Population Biology, Mariculture Committee CM, CC 14-20Google Scholar
  49. Greenfield DI, Lonsdale DJ (2002) Mortality and growth of juvenile hard clams Mercenaria mercenaria during brown tide. Mar Biol 141:1045–1050Google Scholar
  50. Guillard RRL (1959) Further evidence of the destruction of bivalve larvae by bacteria. Biol Bull 117:258–266Google Scholar
  51. Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, D’Agrosa C et al (2008) A global map of human impact on marine ecosystems. Science 319:948–952Google Scholar
  52. Hartmann DL, Klein Tank AMG, Rusticucci M (2013) Observation: atmosphere and surface. IPCC WGI AR5 (Report). p 198Google Scholar
  53. Harvell D, Altizer S, Cattadori IM, Harrington L, Weil E (2009) Climate change and wildlife diseases: when does the host matter the most? Ecology 90:912–920Google Scholar
  54. Hegaret H, Wikfors GH (2005) Effects of natural and field simulated blooms of the dinoflagellate Prorocentrum minimum upon hemocytes of eastern oysters, Crassostrea virginica, from two different populations. Harmful Algae 4:201–209Google Scholar
  55. Hégaret H, Wikfors GH, Soudant P (2003) Flow-cytometric analysis of hemocytes from eastern oysters, Crassostrea virginica, subjected to a sudden temperature elevation: II. Hemocyte functions: aggregation, viability, phagocytosis and respiratory burst. J Exp Mar Biol Ecol 293:249–265Google Scholar
  56. Hine PM (1997) Trends in research on diseases of bivalve mollusks. Bulletin of the European Association of Fish Pathologists 17:180–183Google Scholar
  57. Hine PM, Thorne ET (1997) Replication of herpes-like viruses in haemocytes of adult flat oysters Ostrea angasi: an ultrastructural study. Dis Aquat Organ 29:189–196Google Scholar
  58. Hine PM, Wesney B, Hay BE (1992) Herpesviruses associated with mortalities among hatchery-reared Pacific oysters, Crassostrea gigas. Dis Aquat Organ 12:135–142Google Scholar
  59. Hofmann EE, Bushek D, Ford SE, Guo X (2009) Understanding how disease and environment combine to structure resistance in estuarine bivalve population. CCPO Publications. Paper 33Google Scholar
  60. Huvet A, Herpin A, Degremont L, Labreuche Y, Samain JF, Cunningham C (2004) The identification of genes from the oyster Crassostrea gigas that are differentially expressed in progeny exhibiting opposed susceptibility to summer mortality. Gene 343(1):211–220Google Scholar
  61. Ilarri M, Antunes C, Guilhermino L, Sousa R (2011) Massive mortality of the Asian clam Corbicula fluminea in a highly invaded area. Biol Invasions 13:277–280Google Scholar
  62. IPCC (2007) Summary for policymakers. In: Solomon et al (eds) Climate change 2007: the physical science basis. Contribution of Working Group I to the fourth assessment report of the Intergovernmental Panel on Climate Change, Cambridge University Press, CambridgeGoogle Scholar
  63. Ivanina AV, Dickinson GH, Matoo OB, Bagwe R, Dickinson A, Beniash E, Sokolova IM (2013) Interactive effects of elevated temperature and CO2 levels on energy metabolism and biomineralization of marine bivalves Crassostrea virginica and Mercenaria mercenaria. Comp Biochem Physiol A Mol Integr Physiol 166(1):101–111Google Scholar
  64. Joint I, Smale DA (2017) Marie heat waves and optimal temperatures for microbial assemblage activity. FEMS Microbiol Ecol 93(2)Google Scholar
  65. Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434Google Scholar
  66. Kroeker KJ, Kordas RL, Crim RN, Hendriks IE, Ramajo L, Singh GS, Duarte CM, Gattuso JP (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Chang Biol 19:1884–1896Google Scholar
  67. Lacoste A, Jalabert F, Malham S, Cueff A, Gélébart F, Cordevant C, Lange M, Poulet SA (2001) A vibrio splendidus strain is associated with summer mortality of juvenile oysters Crassostrea gigas in the Bay of Morlaix (North Brittany, France). Dis Aquat Organ 46:139–145Google Scholar
  68. Lan Y, Ye T, Xue Y, Liu H, Zhang H, Cheng D, Zhao M, Zhang Y, Li S, Ma H, Zheng H (2018) Physiological and immunological responses to mass mortality in noble scallop Chlamys nobilis cultured in Nan’ao waters of Shantou, China. Fish Shellfish Immunol 82:453–459Google Scholar
  69. Landsberg JH (2002) The effects of harmful algal blooms on aquatic organisms. Rev Fish Sci 10:113–390Google Scholar
  70. Lauckner G (1983) Diseases of mollusca: Bivalvia. In: Kinne O (ed) Diseases of marine animals volume II: introduction, Bivalvia to Scaphopoda. Biologische Anstalt Helgoland, Hamburg, pp 477–961Google Scholar
  71. Leibovitz L, Schott EF, Karney RC (1984) Diseases of wild, captive and cultured scallops. J World Mariculture Soc 15(1):269–283Google Scholar
  72. Leverone JR, Shumway SE, Blake NJ (2007) Comparative effects of the toxic dinoflagellate Karenia brevis on clearance rates in juvenile of four bivalve molluscs from Florida, USA. Toxicon 49(5):634–645Google Scholar
  73. Li Y, Qin JG, Abbott CA, Li XX, Benkendorff K (2007) Synergistic impacts of heat shock and spawning on the physiology and immune health of Crassostrea gigas: an explanation for summer mortality in Pacific oysters. Am J Physiol 293:2353–2362Google Scholar
  74. Li S, Liu C, Huang J, Liu Y, Zheng G, Xie L, Zhang R (2015) Interactive effects of seawater acidification and elevated temperature on biomineralization and amino acid metabolism in the mussel Mytilus edulis. J Exp Biol 218:3623–3631Google Scholar
  75. Lough JM, Hobday AJ (2011) Observed climate change in Australian marine and freshwater environments. Mar Freshw Res 62:984–999Google Scholar
  76. Luckenbach MW, Sellner KG, Shumway SE, Greene K (1993) Effects of two bloom-forming dinoflagellates, Prorocentrum minimum and Gyrodinium uncatenum, on the growth and survival of the eastern oyster, Crassostrea virginica (Gmelin 1791). J Shellfish Res 12:411–415Google Scholar
  77. Lynch SA, Carlson J, Reilly AO, Cotter E, Culloty SC (2012) A previously undescribed ostreid herpesvirus 1 (OsHV-1) genotype detected in the Pacific oyster, Crassostrea gigas, in Ireland. Parasitology 139:1526–1532Google Scholar
  78. Mackin JG, Owen HM, Collier A (1950) Preliminary note on the occurrence of a new protistan parasite, Dermocystidium marinum n. sp. in Crassostrea virginica (Gmelin). Science 111:328–329Google Scholar
  79. Malham SK, Cotter E, O’Keeffe S, Lynch S, Culloty SC, King JW, Latchford JW, Beaumont AR (2010) Summer mortality of the Pacific oyster, Crassostrea gigas, in the Irish Sea: The influence of temperature and nutrients on health and survival. Aquaculture 287(1–2):128–138Google Scholar
  80. Malham SK, Hutchinson TH, Longshaw M (2012) A review of the biology of European cockles (Cerastoderma spp.). J Marine Biol Assoc UK 92:1563–1577Google Scholar
  81. Maloy AP, Ford SE, Karney RC, Boettcher KJ (2007) Roseovarius crassostreae, the etiological agent of Juvenile Oyster Disease (now to be known as Roseovarius Oyster Disease) in Crassostrea virginica. Aquaculture 269:71–83Google Scholar
  82. Matsuyama Y (1999) Harmful effect of dinoflagellate Heterocapsa cicularisquama on shellfish aquaculture in Japan. Jpn Agr Res Q 33:283–293Google Scholar
  83. Matsuyama Y (2012) Impacts of the harmful dinoflagellate Heterocapsa circularisquama bloom on shellfish aquaculture in Japan and some experimental studies on invertebrates. Harmful Algae 14:144–155Google Scholar
  84. Matsuyama Y, Nagai K, Mizuguchi T, Fujiwara M, Ishimura M, Yamaguchi M, Uchida T, Honjo T (1995) Ecological features and mass mortality of pearl oysters during the red tide of Heterocapsa sp. in Ago Bay in 1992. Nippon Suisan Gakk 61:35–41Google Scholar
  85. Matsuyama Y, Uchida T, Nagai K, Ishimura M, Nishimura A, Yamaguchi M, Honjo T (1996) Harmful and toxic algal blooms. In: Yasumoto T, Oshima Y, Fukuyo Y (eds) Intergovernmental Oceanographic Commission of UNESCO, pp 247–250Google Scholar
  86. Matthews MA, McMahon RF (1999) Effects of temperature and temperature acclimation on survival of zebra mussel (Dreissena polymorpha) and Asian clams (Corbicula fluminea) under extreme hypoxia. J Moll Stud 65:317–325Google Scholar
  87. McFarland K, Jean F, Thebault J, Volety AK (2016) Potential impacts of blooms of the toxic dinoflagellate Karenia brevis on the growth, survival and juvenile recruitment of the non-native green mussel Perna viridis in Southeastern United States. Toxicon 109:94–102Google Scholar
  88. Millero FJ, Woosley R, Ditrolio B, Waters J (2009a) Effects of ocean acidification on the speciation of metals in seawater. Oceanogr Mar Biol Annu Rev 22:72–85Google Scholar
  89. Millero F, Woosley R, DiTrolio B, Waters J (2009b) Effect of ocean acidification on the speciation of metals in seawater. Oceanography 22(4):72–85Google Scholar
  90. Monari M, Matozzo V, Foschi J, Cattani O, Serrazanetti GP, Marin MG (2007) Effects of high temperatures on functional responses of haemocytes in the clam Chamelea gallina. Fish Shellfish Immunol 22:98–114Google Scholar
  91. Mouthon J, Daufesne M (2006) Effects of the 2003 heatwave and climate warning on mollusc communities of the Saone: a large lowland river and of its two main tributaries (France). Glob Chang Biol 12:441–449Google Scholar
  92. Nicolas JL, Comps M, Cochennec N (1992) Herpes-like virus infecting Pacific oyster larvae, Crassostrea gigas. Bull Eur Assoc Fish Pathol 12(1):11–13Google Scholar
  93. Nicolas J, Corre S, Gautheir G, Robert R, Ansquer D (1996) Bacterial problems associated with scallop Pecten maximus larval culture. Dis Aquat Organ 27:67–76Google Scholar
  94. O’Donnell M, George MN, Carrington E (2013) Mussel byssus attachment weakened by ocean acidification. Nat Clim Chang 3:587–590Google Scholar
  95. Ortega L, Celentano E, Delgado E, Defeo O (2016) Climate change influences on abundance, individual size and body abnormalities in a sandy beach clam. Mar Ecol Prog Ser 545:203–213Google Scholar
  96. Park KI, Yang HS, Kang HS, Cho M, Park KJ, Choi KS (2010) Isolation and identification of Perkinsus olseni from feces and marine sediment using immunological and molecular techniques. J Invertebr Pathol 105:261–269Google Scholar
  97. Paynter KT, Politano V, Lane HA, Allen SM, Meritt D (2010) Growth rates and prevalence of Perkinsus marinus in restored oyster populations in Maryland. J Shellfish Res 29:309–317Google Scholar
  98. Peeler JE, Reese RA, Cheslett DL, Geoghegan F, Power A, Trush MA (2012) Investigation of mortality in Pacific oysters associated with Ostreid herpesvirus-1 μVar in the Republic of Ireland in 2009. Prev Vet Med 105:136–143Google Scholar
  99. Queiroga FR, Vianna RT, Vieira CB, Farias ND, Da Silva PM (2015) Parasites infecting the cultured oyster Crassostrea gasar (Adanson, 1757) in Northeast Brazil. Parasitology 142:756–766Google Scholar
  100. Ramakritinan CM, Chandurvelan R, Kumaraguru AK (2012) Acute toxicity of metals: Cu, Pb, Cd, Hg and Zn on marine molluscs, Cerithidea cingulate G., and Modiolus philippinarum H. Indian J Geomarine Sci 41(2):141–145Google Scholar
  101. Remacha-Trivino A, Borsay-Horowitz D, Dungan C, Gual-Arnau X, Gomez-Leon J, Villamil L, Gomez-Chiarri M (2008) Numerical quantification of Perkinsus marinus in the American oyster Crassostrea virginica (Gmelin, 1791) (Mollusca: Bivalvia) by modern stereology. J Parasitol 94:125–136Google Scholar
  102. Renault T, Cochennec N, Le Deuff RM, Chollet B (1994a) Herpes-like virus infecting Japanese oyster (Crassostrea gigas) spat. Bull Eur Assoc Fish Pathol 14:64–66Google Scholar
  103. Renault T, Le Deuff RM, Cochennec N, Maffart P (1994b) Herpesviruses associated with mortalities among Pacific oyster, Crassostrea gigas, in France – comparative study. Rev Med Vet 145:735–742Google Scholar
  104. Renault T, Chollet B, Cochennec N, Gerard A (2002) Shell disease in eastern oysters, Crassostrea virginica, reared in France. J Invertebr Pathol 79:1–6Google Scholar
  105. Renault T, Moreau P, Faury N, Pepin JF, Segarra A, Webb S (2012) Analysis of clinical ostreid herpesvirus 1 (Malacoherpesviridae) specimens by sequencing amplified fragments from three virus genome areas. J Virol 86:5942–5947Google Scholar
  106. Sabine CL, Feely RA, Gruber N, Key RM, Lee K, Bullister JL, Wanninkhof R, Wong CS, Wallace DWR, Tilbrook B, Millero FJ, Peng TH, Kozyr A, Ono T, Rios AF (2004) The oceanic sink for anthropogenic CO2. Science 305:367–371Google Scholar
  107. Saulnier D, De Decker S, Haffner P, Cobret L, Robert M, Garcia C (2010) A large scale epidemiological study to identify bacteria pathogenic to pacific oyster Crassostrea gigas and correlation between virulence and metalloprotease-like activity. Microb Ecol 59:787–798Google Scholar
  108. Segarra A, Pepin JF, Arzul I, Morga B, Faury N, Renault T (2010) Detection and description of a particular Ostreid herpesvirus 1 genotype associated with massive mortality outbreaks of Pacific oysters, Crassostrea gigas. Virus Res 153:92–95Google Scholar
  109. Sellner KG, Shumway SE, Luckenbach MW, Cucci TL (1995) The effects of dinoflagellate blooms on the oyster Crassostrea virginica in Chesapeake Bay. In: Lassus P, Arzul G, Erard-LeDen E, Gentien P, Marcaillou-LeBaut C (eds) Harmful algal blooms. Lavoisier, Paris, pp 505–512Google Scholar
  110. Shi W, Zhao X, Han Y, Che Z, Chai X, Liu G (2016) Ocean acidification increases cadmium accumulation in marine bivalves: a potential threat to seafood safety. Sci Rep 6:20197Google Scholar
  111. Shirayama Y, Thornton H (2005) Effect of increased atmospheric CO2 on shallow water marine benthos. J Geophys Res Oceans 110:C09S08Google Scholar
  112. Smolowitz R (2013) A review of current state of knowledge concerning Perkinsus Marinus effects on Crassostrea virginica (Gmelin) (the eastern oyster). Vet Pathol 50:404–411Google Scholar
  113. Soletchnik P, Ropert M, Mazurié J, Fleury PG, Le Coz F (2007) Relationships between oyster mortality patterns and environmental data from monitoring databases along the coasts of France. Aquaculture 271(1–4):384–400Google Scholar
  114. Soniat TM (1996) Epizootiology of Perkinsus marinus disease of eastern oysters in the Gulf of Mexico. J Shellfish Res 15:35–43Google Scholar
  115. Talmage SC, Gobler CJ (2011) Effects of elevated temperature and carbon dioxide on the growth and survival of larvae and juveniles of three species of Northwest Atlantic bivalves. PLoS One 6(10):e26941Google Scholar
  116. Tan KS, Ransangan J (2015) Factors influencing the toxicity, detoxification and biotransformation of paralytic shellfish toxins. In: Whitacre DM (ed) Reviews of environmental contamination and toxicology volume 235. Springer International Publishing Switzerland, Basel, pp 1–25Google Scholar
  117. Tan KS, Ransangan J (2016a) Feeding behaviour of green mussels, Perna viridis in Marudu Bay, Malaysia. Aquacult Res 48(3):1216–1231Google Scholar
  118. Tan KS, Ransangan J (2016b) Feasibility of green mussel, Perna viridis farming in Marudu Bay, Malaysia. Aquac Rep 4:130–135Google Scholar
  119. Tan KS, Ransangan J (2016c) High mortality and poor growth of green mussels, Perna viridis, in high chlorophyll-a environment. Ocean Sci J 51(1):43–57Google Scholar
  120. Tan KS, Ransangan J (2016d) Effects of environmental conditions and nutrients on the occurrence and distribution of potentially harmful phytoplankton in mesotrophic water. Sains Malaysiana 45(6):865–877Google Scholar
  121. Tan KS, Ransangan J (2017) Effects of nutrients and zooplankton on the phytoplankton community structure in Marudu Bay. Estuar Coast Shelf Sci 194:16–29Google Scholar
  122. Thomas MK, Kremer CT, Klausmeier CA, Litchman E (2012) A global pattern of thermal adaptation in marine phytoplankton. Science 338:1085–1088Google Scholar
  123. Tracey GA (1988) Feeding reduction, reproductive failure, and mortality in Mytilus edulis during the 1985 “brown tide” in Narragansett Bay, Rhode Island. Mar Ecol Prog Ser 50:73–81Google Scholar
  124. Tubiash HS, Chanley PE, Leifson E (1965) Bacillary necrosis, a disease of larval and juvenile bivalve mollusks. I. Etiology and epizootiology. J Bacteriol 90:1036–1044Google Scholar
  125. Vohmann A, Borcherding J, Kureek A (2009) Strong body mass decrease of the invasive clam Corbicula fluminea during summer. Biol Invasions 12:53–64Google Scholar
  126. Wazniak CE, Glibert PM (2004) Potential impacts of brown tide, Aureococcus anophagefferens, on juvenile hard clams, Mercenaria mercenaria, in the coastal bays of Maryland, USA. Harmful Algae 3:321–329Google Scholar
  127. Wendling CC, Wegner KM (2013) Relative contribution of reproductive investment, thermal stress and Vibrio infection to summer mortality phenomena in Pacific oysters. Aquaculture 412–413:88–96Google Scholar
  128. Werner S, Rothhauot KO (2008) Mass mortality of the invasive bivalve Corbicula fluminea induced by a severe low-water event and associated low water temperatures. Hydrobiologia 613:143–150Google Scholar
  129. Whyte C, Swan S, Davidson K (2014) Changing wind patterns linked to unusually high Dinophysis blooms around the Shetland Islands, Scotland. Harmful Algae 39:365–373Google Scholar
  130. Wikfors GH (2005) A review and new analysis of trophic interactions between Prorocentrum minimum and clams, scallops, and oysters. Harmful Algae 4:585–592Google Scholar
  131. Wikfors GH, Smolowitz RM (1993) Detrimental effects of a Prorocentrum isolate upon hard clams and bay scallops in laboratory feeding studies. In: Smayda TJ, Shimizu Y (eds) Toxic phytoplankton blooms in the sea. Elsevier, New York, pp 447–452Google Scholar
  132. Wootton EC, Dyrynda EA, Ratcliffe NA (2003) Bivalve immunity: comparisons between the marine mussel (Mytilus edulis), the edible cockle (Cerastoderma edule) and the razor-shell (Ensis siliqua). Fish Shellfish Immunol 15:195–210Google Scholar
  133. Yamamoto C, Tanaka Y (1990) Two species of harmful red tide plankton increased in Fukuoka Bay. Bull Fukuoka Fisheries Exp Station 16:43–44Google Scholar
  134. Yurimoto T, Kassim FM, Fuseya R, Man A (2014) Mass mortality event of the blood cockle, Anadara granosa, in aquaculture ground along Selangor coast, Peninsular Malaysia. Int Aquat Res 6:177–186Google Scholar
  135. Zha S, Liu S, Su W, Shi W, Xiao G, Yan M, Liu G (2017) Laboratory simulation reveals significantly impacts of ocean acidification on microbial community composition and host-pathogen interactions between the blood clam and Vibrio harveyi. Fish Shellfish Immunol 71:393–398Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Key Laboratory of Marine Biotechnology of Guangdong ProvinceShantou UniversityShantouChina

Personalised recommendations