Abstract
Besides human health risks, phycotoxins may cause physiological injuries on molluscan shellfish and, consequently, damages to marine ecosystems and global fisheries production. In this way, this review aimed to present an overview of HABs impacts on marine shellfish by evaluating the effects of cultivated molluscs exposure to microalgae and cyanobacteria that form blooms and/or synthesize toxins. More specifically, it was assessed the main molluscan shellfish responses to harmful algae, trophic transfer and dynamics of phycotoxins, and the risks for human health. Of the 2420 results obtained from literature search, 150 scientific publications were selected after thorough inspections for subject adherence. In total, 70 molluscan species and 37 taxa of harmful algae were assessed from retrieved scientific publications. A significant positive correlation was found between the marine production of molluscs and the number of available studies by molluscan category. Molluscan responses to HABs and phycotoxins were categorized and discussed in three sub-sections: effects on grazing and behavior, metabolic and physiological reactions, and fitness consequences. The main histopathological injuries and toxin concentrations in molluscan tissues were also compiled and discussed. Bivalves often accumulate more toxins than gastropods and cephalopods, occasionally exceeding recommended levels for safe consumption, representing a risk for human health. Harmful algae impact on molluscan shellfish are complex to trace and predict; however, considering the perspective of increase in the occurrence and intensity of HABs, the intensification of efforts to expand the knowledge about HABs impacts on marine molluscs is crucial to mitigate the damages on economy and human health.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article and its supplementary material Table S1.
References
Abouabdellah R, Taleb H, Bennouna A, Erler K, Chafik A, Moukrim A (2008) Paralytic shellfish poisoning toxin profile of mussels Perna perna from southern Atlantic coasts of Morocco. Toxicon 51:780–786. https://doi.org/10.1016/j.toxicon.2007.12.004
Ajani P, Harwood D, Murray S (2017) Recent trends in marine phycotoxins from Australian coastal waters. Mar Drugs 15:33. https://doi.org/10.3390/md15020033
Akberali HB, Trueman ER (1985) Effects of environmental stress on marine bivalve molluscs. Adv Mar Biol 22:101–198. https://doi.org/10.1016/S0065-2881(08)60051-6
Amzil Z, Fresnel J, Le Gal D, Billard C (2001) Domoic acid accumulation in French shellfish in relation to toxic species of Pseudo-nitzschia multiseries and P. pseudodelicatissima. Toxicon 39:1245–1251. https://doi.org/10.1016/s0041-0101(01)00096-4
Anderson DM, Alpermann TJ, Cembella AD, Collos Y, Masseret E, Montresor M (2012) The globally distributed genus Alexandrium: multifaceted roles in marine ecosystems and impacts on human health. Harmful Algae 14:10–35. https://doi.org/10.1016/j.hal.2011.10.012
Astuya AP, Carrera C, Ulloa V, Aballay AE, Núñez-Acuña G, Hégaret H, Gallardo-Escárate C (2015) Saxitoxin modulates immunological parameters and gene transcription in Mytilus chilensis hemocytes. Int J Mol Sci 16:15235–15250. https://doi.org/10.3390/ijms160715235
Band-Schmidt CJ, Bustillos-Guzmán J, Gárate-Lizárraga I, Lechuga-Devéze CH, Reinhardt K, Luckas B (2005) Paralytic shellfish toxin profile in strains of the dinoflagellate Gymnodinium catenatum Graham and the scallop Argopecten ventricosus G.B. Sowerby II from Bahía Concepción, Gulf of California, Mexico. Harmful Algae 4:21–31. https://doi.org/10.1016/j.hal.2003.10.004
Barcia R, Ramos-Martínez JI (2011) Stress-based modulation of the immune response in molluscan hemocytes: a two-receptor model. ISJ- Invert Surviv J 8:56–58
Bargu S, Powell CL, Wang Z, Doucette GJ, Silver MW (2008) Note on the occurrence of Pseudo-nitzschia australis and domoic acid in squid from Monterey Bay, CA (USA). Harmful Algae 7:45–51. https://doi.org/10.1016/j.hal.2007.05.008
Basti L, Segawa S (2010) Mortality of the short-neck clam Ruditapes philippinarum induced by the toxic dinoflagellate Heterocapsa circularisquama. Fish Sci 76:625–631. https://doi.org/10.1007/s12562-010-0252-4
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 291:41–47. https://doi.org/10.1016/j.aquaculture.2009.02.029
Basti L, Endo M, Segawa S (2011a) Physiological, pathological, and defense alterations in Manila clams (short-neck clams), Ruditapes philippinarum, induced by Heterocapsa circularisquama. J Shellfish Res 30:829–844. https://doi.org/10.2983/035.030.0324
Basti L, Go J, Higuchi K, Nagai K, Segawa S (2011b) Effects of the toxic dinoflagellate Heterocapsa circularisquama on larvae of the Pearl Oyster Pinctada fucata martensii (Dunker, 1873). J Shellfish Res 30:177–186. https://doi.org/10.2983/035.030.0125
Basti L, Nagai K, Tanaka Y, Segawa S (2013) Sensitivity of gametes, fertilization, and embryo development of the Japanese pearl oyster, Pinctada fucata martensii, to the harmful dinoflagellate, Heterocapsa circularisquama. Mar Biol 160:211–219. https://doi.org/10.1007/s00227-012-2079-2
Basti L, Uchida H, Kanamori M, Matsushima R, Suzuki T, Nagai S (2014a) Mortality and pathology of Japanese scallop, Patinopecten (Mizuhopecten) yessoensis, and noble scallop, Mimachlamys nobilis, fed monoclonal culture of PTX-producer, Dinophysis caudata. In: AL MK (ed) Proceedings of the 16th International Conference on Harmful Algae. Cawthron Institute and the International Society for the Study of Harmful Algae (ISSHA), New Zealand, pp 105–108
Basti L, Nagai S, Nagai K, Go J, Okano S, Watanabe R, Suzuki T, Tanaka Y (2014b) Harmful algal blooms affect early life-stages of Japanese pearl oyster, Pinctada fucata martensii. In: AL MK (ed) Proceedings of the 16th International Conference on Harmful Algae. Cawthron Institute and the International Society for the Study of Harmful Algae (ISSHA), New Zealand, pp 94–97
Basti L, Nagai S, Go J, Okano S, Nagai K, Watanabe R, Suzuki T, Tanaka Y (2015a) Differential inimical effects of Alexandrium spp. and Karenia spp. on cleavage, hatching, and two larval stages of Japanese pearl oyster Pinctada fucata martensii. Harmful Algae 43:1–12. https://doi.org/10.1016/j.hal.2014.12.004
Basti L, Endo M, Segawa S, Shumway SE, Tanaka Y, Nagai S (2015b) Prevalence and intensity of pathologies induced by the toxic dinoflagellate, Heterocapsa circularisquama, in the Mediterranean mussel, Mytilus galloprovincialis. Aquat Toxicol 163:37–50. https://doi.org/10.1016/j.aquatox.2015.03.012
Basti L, Nagai S, Watanabe S, Oda T, Tanaka Y (2016) Neuroenzymatic activity and physiological energetics in Manila clam, Ruditapes philippinarum, during short-term sublethal exposure to harmful alga, Heterocapsa circularisquama. Aquat Toxicol 176:76–87. https://doi.org/10.1016/j.aquatox.2016.04.011
Basti L, Hégaret H, Shumway SE (2018) Harmful algal blooms and shellfish. In: Shumway SE, Burkholder JM, Morton SL (eds) Harmful algal blooms: a compendium desk reference. Wiley, Chichester, pp 135–190. https://doi.org/10.1002/9781118994672.ch4
Berger VJ, Kharazova AD (1997) Mechanisms of salinity adaptations in marine molluscs. Hydrobiologia 355:115–126. https://doi.org/10.1023/A:1003023322263
Blanco J (2006) Modelling phycotoxins accumulation in bivalves: a review. In: Henshilwood K (ed) Proceedings of the fifth International Conference on Molluscan Shellfish Safety. Marine Institute, California, pp 258–269
Blanco J, Moroño A, Franco J, Reyero MI (1997) PSP detoxification kinetics in the mussel Mytilus galloprovincialis. One and two-compartment models and the effect of some environmental variables. Mar Ecol Prog Ser 158:165–175
Blanco J, Moroño A, Fernandez ML (2005) Toxic episodes in shellfish produced by lipohilic phycotoxins: an overview. Revista Galega de Recursos Mariños 1:1–70
Bogan YM, Harkin AL, Gillespie J, Kennedy DJ, Hess P, Slater JW (2007a) The influence of size on domoic acid concentration in king scallop, Pecten maximus (L.). Harmful Algae 6:15–28. https://doi.org/10.1016/j.hal.2006.05.005
Bogan YM, Kennedy DJ, Harkin AL, Gillespie J, Vause BJ, Beukers-Stewart BD, Hess P, Slater JW (2007b) Variation in domoic acid concentration in king scallop (Pecten maximus) from fishing grounds around the Isle of Man. Harmful Algae 6:81–92. https://doi.org/10.1016/j.hal.2006.07.002
Borcier E, Morvezen R, Boudry P, Miner P, Charrier GG, Laroche J, Hégaret H (2017) Effects of bioactive extracellular compounds and paralytic shellfish toxins produced by Alexandrium minutum on growth and behaviour of juvenile great scallops Pecten maximus. Aquat Toxicol 184:142–154. https://doi.org/10.1016/j.aquatox.2017.01.009
Branch GM, Bustamante RH, Robinson TB (2013) Impacts of a “black tide” harmful algal bloom on rocky-shore intertidal communities on the West Coast of South Africa. Harmful Algae 24:54–64. https://doi.org/10.1016/j.hal.2013.01.005
Bricelj VM, Shumway SE (1998) Paralytic shellfish toxins in bivalve molluscs: occurrence, transfer kinetics, and biotransformation. Rev Fish Sci 6:315–383. https://doi.org/10.1080/10641269891314294
Bricelj V, Cembella A, Laby D, Shumway S, Cucci T (1996) Comparative physiological and behavioral responses to PSP toxins in two bivalve molluscs, the softshell clam, Mya arenaria, and surfclam Spisula solidissima. In: Yasumoto T, Oshima Y, Fukuyo Y (eds) Harmful and Toxic Algal Blooms. UNESCO, Japan, pp 405–408
Bricelj VM, Connell L, Konoki K, MacQuarrie SP, Scheuer T, Catterall WA, Trainer VL (2005) Sodium channel mutation leading to saxitoxin resistance in clams increases risk of PSP. Nature 434:763–767. https://doi.org/10.1038/nature03415
Bricelj VM, MacQuarrie SP, Doane JAE, Connell LB (2010) Evidence of selection for resistance to paralytic shellfish toxins during the early life history of soft-shell clam (Mya arenaria) populations. Limnol Oceanogr 55:2463–2475. https://doi.org/10.4319/lo.2010.55.6.2463
Bricelj VM, Haubois AG, Sengco MR, Pierce RH, Culter JK, Anderson DM (2012) Trophic transfer of brevetoxins to the benthic macrofaunal community during a bloom of the harmful dinoflagellate Karenia brevis in Sarasota Bay, Florida. Harmful Algae 16:27–34. https://doi.org/10.1016/j.hal.2012.01.001
Cabado AG, Lago J, González V, Blanco L, Paz B, Diogène J, Ferreres L, Rambla-Alegre M (2020) Detoxification of paralytic shellfish poisoning toxins in naturally contaminated mussels, clams and scallops by an industrial procedure. Food Chem Toxicol 141:111386. https://doi.org/10.1016/j.fct.2020.111386
Carella F, Sardo A, Mangoni O, Di Cioccio D, Urciuolo G, De Vico G, Zingone A (2015) Quantitative histopathology of the Mediterranean mussel (Mytilus galloprovincialis L.) exposed to the harmful dinoflagellate Ostreopsis cf. ovata. J Invertebr Pathol 127:130–140. https://doi.org/10.1016/j.jip.2015.03.001
Carreto JI, Elbusto C, Sancho H, Carignan M, Yasumoto T, Oshima Y (1996) Comparative studies on paralytic shellfish toxin profiles of marine snails, mussels and an Alexandium tamarense isolate from The Mar del Plata Coast (Argentina). Rev Invest Desarr Pesq 10:101–107
Castrec J, Soudant P, Payton L, Tran D, Miner P, Lambert C, Le Goïc N, Huvet A, Quillien V, Boullot F, Amzil Z, Hégaret H, Fabioux C (2018) Bioactive extracellular compounds produced by the dinoflagellate Alexandrium minutum are highly detrimental for oysters. Aquat Toxicol 199:188–198. https://doi.org/10.1016/j.aquatox.2018.03.034
Chen CY, Chou HN (1998) Transmission of the paralytic shellfish poisoning toxins, from dinoflagellate to gastropod. Toxicon 36:515–522. https://doi.org/10.1016/s0041-0101(97)00093-7
Chen CY, Chou HN (2001) Accumulation and depuration of paralytic shellfish poisoning toxins by purple clam Hiatula rostrata Lighttoot. Toxicon 39:1029–1034. https://doi.org/10.1016/s0041-0101(00)00242-7
Choi MC, Hsieh DPH, Lam PKS, Wang WX (2003) Field depuration and biotransformation of paralytic shellfish toxins in scallop Chlamys nobilis and green-lipped mussel Perna viridis. Mar Biol 143:927–934. https://doi.org/10.1007/s00227-003-1148-y
Connell LB, MacQuarrie SP, Twarog BM, Iszard M, Bricelj VM (2007) Population differences in nerve resistance to paralytic shellfish toxins in softshell clam, Mya arenaria, associated with sodium channel mutations. Mar Biol 150:1227–1236. https://doi.org/10.1007/s00227-006-0432-z
Contreras AM, Marsden ID, Munro MHG (2012) Physiological effects and biotransformation of PSP toxins in the New Zealand scallop, Pecten novaezelandiae. J Shellfish Res 31:1151–1159. https://doi.org/10.2983/035.031.0426
Costa PR (2016) Impact and effects of paralytic shellfish poisoning toxins derived from harmful algal blooms to marine fish. Fish Fish 17:226–248. https://doi.org/10.1111/faf.12105
Costa PR, Rosa R, Sampayo MAM (2004) Tissue distribution of the amnesic shellfish toxin, domoic acid, in Octopus vulgaris from the Portuguese coast. Mar Biol 144:971–976. https://doi.org/10.1007/s00227-003-1258-6
Costa PR, Rosa R, Duarte-Silva A, Brotas V, Sampayo MAM (2005) Accumulation, transformation and tissue distribution of domoic acid, the amnesic shellfish poisoning toxin, in the common cuttlefish, Sepia officinalis. Aquat Toxicol 74:82–91. https://doi.org/10.1016/j.aquatox.2005.01.011
Costa PR, Botelho MJ, Rodrigues SM (2009) Accumulation of paralytic shellfish toxins in digestive gland of Octopus vulgaris during bloom events including the dinoflagellate Gymnodinium catenatum. Mar Pollut Bull 58:1747–1750. https://doi.org/10.1016/j.marpolbul.2009.08.005
Costello KE, Lynch SA, O’Riordan RM, McAllen R, Culloty SC (2021) The importance of marine bivalves in invasive host–parasite introductions. Front Mar Sci 8:1–14. https://doi.org/10.3389/fmars.2021.609248
Couch JA, Fournie JW (2021) Pathobiology of marine and estuarine organisms. Advances in Fisheries Science Book 2, CRC Press, 555 p.
Cuevas N, Zorita I, Costa PM, Franco J, Larreta J (2015) Development of histopathological indices in the digestive gland and gonad of mussels: integration with contamination levels and effects of confounding factors. Aquat Toxicol 162:152–164. https://doi.org/10.1016/j.aquatox.2015.03.011
da Silva PM, Hégaret H, Lambert C, Wikfors GH, Le Goïc N, Shumway SE, Soudant P (2008) Immunological responses of the Manila clam (Ruditapes philippinarum) with varying parasite (Perkinsus olseni) burden, during a long-term exposure to the harmful alga, Karenia selliformis, and possible interactions. Toxicon 51:563–573. https://doi.org/10.1016/j.toxicon.2007.11.006
Deeds J, Landsberg J, Etheridge S, Pitcher G, Longan S (2008) Non-traditional vectors for paralytic shellfish poisoning. Mar Drugs 6:308–348. https://doi.org/10.3390/md6020308
Dizer H, Fischer B, Harabawy ASA, Hennion MC, Hansen PD (2001) Toxicity of domoic acid in the marine mussel Mytilus edulis. Aquat Toxicol 55:149–156. https://doi.org/10.1016/s0166-445x(01)00178-3
Doucette G, Maneiro I, Riveiro I, Svensen C (2006) Phycotoxin pathways in aquatic food webs: transfer, accumulation and degradation. In: Granéli E, Turner J (eds) Ecology of harmful algae. Ecological Studies, vol 189. Springer, Berlin, Heidelberg, pp 283–295
Dowsett N, Hallegraeff G, Van Ruth P, Van Ginkel R, McNabb P, Hay B, O’Connor W, Kiermeier A, Deveney M, McLeod C (2011) Uptake, distribution and depuration of paralytic shellfish toxins from Alexandrium minutum in Australian greenlip abalone, Haliotis laevigata. Toxicon 58:101–111. https://doi.org/10.1016/j.toxicon.2011.05.010
Duan GF, Liu Y, Zhang LN, Li HY, Liu JS, Yang WD (2021) Cinnamaldehyde could reduce the accumulation of diarrhetic shellfish toxins in the digestive gland of the mussel Perna viridis under laboratory conditions. Mar Drugs 19:63. https://doi.org/10.3390/md19020063
Echevarria M, Naar JP, Tomas C, Pawlik JR (2012) Effects of Karenia brevis on clearance rates and bioaccumulation of brevetoxins in benthic suspension feeding invertebrates. Aquat Toxicol 106–107:85–94. https://doi.org/10.1016/j.aquatox.2011.10.011
Escobedo-Lozano AY, Estrada N, Ascencio F, Contreras G, Alonso-Rodriguez R (2012) Accumulation, biotransformation, histopathology and paralysis in the pacific calico scallop Argopecten ventricosus by the paralyzing toxins of the dinoflagellate Gymnodinium catenatum. Mar Drugs 10:1044–1065. https://doi.org/10.3390/md10051044
Estrada N, De Jesús RM, Campa-Córdova A, Luna A, Ascencio F (2007) Effects of the toxic dinoflagellate, Gymnodinium catenatum on hydrolytic and antioxidant enzymes, in tissues of the giant lions-paw scallop Nodipecten subnodosus. Comp Biochem Physiol C Toxicol Pharmacol 146:502–510. https://doi.org/10.1016/j.cbpc.2007.06.003
Estrada N, Ascencio F, Shoshani L, Contreras RG (2014) Apoptosis of hemocytes from lions-paw scallop Nodipecten subnodosus induced with paralyzing shellfish poison from Gymnodinium catenatum. Immunobiology 219:964–974. https://doi.org/10.1016/j.imbio.2014.07.006
European Commission (2004) Commission regulation (EU) No 853/2004 of the European Parliament and of the Council of 29 April 20004 laying down specific hygiene rules for on the hygiene of foodstuffs. Official Journal of the European Union, L 139/55.
European Commission (2013) Commission regulation (EU) No 786/2013 of the European Parliament and of the Council of 16 August 2013 amending Annex III to Regulation (EC) No 853/2004 as regards the permitted limits of yessotoxins in live bivalve molluscs. Official Journal of the European Union, L 220/14.
Fabioux C, Sulistiyani Y, Haberkorn H, Hégaret H, Amzil Z, Soudant P (2015) Exposure to toxic Alexandrium minutum activates the detoxifying and antioxidant systems in gills of the oyster Crassostrea gigas. Harmful Algae 48:55–62. https://doi.org/10.1016/j.hal.2015.07.003
Faimali M, Giussani V, Piazza V, Garaventa F, Corrà C, Asnaghi V, Privitera D, Gallus L, Cattaneo-Vietti R, Mangialajo L, Chiantore M (2012) Toxic effects of harmful benthic dinoflagellate Ostreopsis ovata on invertebrate and vertebrate marine organisms. Mar Environ Res 76:97–107. https://doi.org/10.1016/j.marenvres.2011.09.010
FAO - Food and Agriculture Organization of the United Nations (2004) Marine biotoxins. FAO Food and Nutrition Paper 80, Rome. http://www.fao.org/3/a-y5486e.pdf
FAO - Food and Agriculture Organization of the United Nations (2006-2020) Fisheries and aquaculture software. FishStat Plus - Universal software for fishery statistical time series. In: FAO Fisheries and Aquaculture Department. Rome. http://www.fao.org/fishery/
FAO - Food and Agriculture Organization of the United Nations (2012) The state of world fisheries and aquaculture. FAO Fisheries and Aquaculture Department, Rome http://www.fao.org/docrep/016/i2727e/i2727e.pdf
FAO - Food and Agriculture Organization of the United Nations (2014) The state of world fisheries and aquaculture. FAO Fisheries and Aquaculture Department, Rome http://www.fao.org/3/a-i3720e.pdf
FAO - Food and Agriculture Organization of the United Nations (2016) AQUASTAT Main Database, FAO. Website accessed on 18/07/2020.
FAO - Food and Agriculture Organization of the United Nations (2019) FAO yearbook. Fishery and Aquaculture Statistics 2017, Rome. ISBN 978-92-5-131669-6. http://www.fao.org/fishery/static/Yearbook/YB2017_USBcard/index.htm
FAO and WHO - Food and Agriculture Organization of the United Nations/World Health Organization (2020) Report of the expert meeting on ciguatera poisoning, Rome, 19-23 November 2018. Food Safety and Quality n° 9, Rome. https://doi.org/10.4060/ca8817en
FAO/IOC/WHO- Food and Agriculture Organization of the United Nations/ Intergovernmental Oceanographic Commission of UNESCO/ World Health Organization (2004) Report of the joint FAO/IOC/WHO ad hoc expert consultation on biotoxins in bivalve molluscs. FAO/IOC/WHO, Oslo http://ftp.fao.org/es/esn/food/biotoxin_report_en.pdf
Fast MD, Cembella AD, Ross NW (2006) In vitro transformation of paralytic shellfish toxins in the clams Mya arenaria and Protothaca staminea. Harmful Algae 5:79–90. https://doi.org/10.1016/j.hal.2005.05.005
FDA - U.S. Food and Drug Administration (2017) National Shellfish Sanitation Program (NSSP) – Guide for the control of molluscan shellfish. http://www.fda.gov/Food/GuidanceRegulation/FederalStateFoodPrograms/ucm2006754.htm
Fernández ML, Shumway SE, Blanco J (2004) Management of shellfish resources. In: Hallegraef GM, Anderson DM, Cembella AD (eds) Manual of Harmful Marine Microalgae. UNESCO, Paris, pp 657–692
Flórez-Barrós F, Prado-Alvarez M, Méndez J, Fernández-Tajes J (2011) Evaluation of genotoxicity in gills and hemolymph of clam Ruditapes decussatus fed with the toxic dinoflagellate Prorocentrum lima. J Toxicol Environ Health A 74:971–979. https://doi.org/10.1080/15287394.2011.582025
Ford SE, Bricelj VM, Lambert C, Paillard C (2008) Deleterious effects of a nonPST bioactive compound(s) from Alexandrium tamarense on bivalve hemocytes. Mar Biol 154:241–253. https://doi.org/10.1007/s00227-008-0917-z
Furey A, Moroney C, Magdalena ABA, Fidalgo Saez MJ, Lehane M, James KJ (2003) Geographical, temporal, and species variation of the polyether toxins, azaspiracids, in shellfish. Environ Sci Technol 37:3078–3084. https://doi.org/10.1021/es020246z
Gainey LF Jr, Shumway SE (1988) A compendium of the responses of bivalve molluscs to toxic dinoflagellates. J Shellfish Res 7:623–628
Galimany E, Place AR, Ramón M, Jutson M, Pipe RK (2008a) The effects of feeding Karlodinium veneficum (PLY # 103; Gymnodinium veneficum Ballantine) to the blue mussel Mytilus edulis. Harmful Algae 7:91–98. https://doi.org/10.1016/j.hal.2007.05.004
Galimany E, Sunila I, Hégaret H, Ramón M, Wikfors GH (2008b) Pathology and immune response of the blue mussel (Mytilus edulis L.) after an exposure to the harmful dinoflagellate Prorocentrum minimum. Harmful Algae 7:630–638. https://doi.org/10.1016/j.hal.2008.01.001
Galimany E, Sunila I, Hégaret H, Ramón M, Wikfors GH (2008c) Experimental exposure of the blue mussel (Mytilus edulis, L.) to the toxic dinoflagellate Alexandrium fundyense: histopathology, immune responses, and recovery. Harmful Algae 7:702–711. https://doi.org/10.1016/j.hal.2008.02.006
Galimany E, Rose JM, Alix J, Dixon MS, Wikfors GH (2014) Responses of the ribbed mussel, Geukensia demissa, to the harmful algae Aureococcus anophagefferens and Heterosigma akashiwo. J Molluscan Stud 80:123–130. https://doi.org/10.1093/mollus/eyt055
Gárate-Lizárraga I, Bustillos-Guzmán JJ, Alonso-Rodríguez R, Luckas B (2004) Comparative paralytic shellfish toxin profiles in two marine bivalves during outbreaks of Gymnodinium catenatum (Dinophyceae) in the Gulf of California. Mar Pollut Bull 48:397–402. https://doi.org/10.1016/j.marpolbul.2003.10.032
García C, Del Carmen Bravo MA, Lagos M, Lagos N (2004) Paralytic shellfish poisoning: post-mortem analysis of tissue and body fluid samples from human victims in the Patagonia fjords. Toxicon 43:149–158. https://doi.org/10.1016/j.toxicon.2003.11.018
García-Lagunas N, Romero-Geraldo R, Hernández-Saavedra NY (2013) Genomics study of the exposure effect of Gymnodinium catenatum, a paralyzing toxin producer, on Crassostrea gigas defense system and detoxification genes. PLoS One 8:e72323. https://doi.org/10.1371/journal.pone.0072323
Glibert PM, Burkholder JM (2006) The complex relationships between increasing fertilization of the earth, coastal eutrophication and proliferation of harmful algal blooms. In: Granéli E, Turner J (eds) Ecology of harmful algae. Springer, Berlin, pp 341–354
Gobler CJ (2020) Climate change and harmful algal blooms: insights and perspective. Harmful Algae 91:101731. https://doi.org/10.1016/j.hal.2019.101731
Granéli E, Vidyarathna NK, Funari E, Cumaranatunga PRT, Scenati R (2011) Can increases in temperature stimulate blooms of the toxic benthic dinoflagellate Ostreopsis ovata? Harmful Algae 10:165–172. https://doi.org/10.1016/j.hal.2010.09.002
Gray JS (2002) Biomagnification in marine systems: the perspective of an ecologist. Mar Pollut Bull 45:46–52. https://doi.org/10.1016/S0025-326X(01)00323-X
Griffith AW, Gobler CJ (2020) Harmful algal blooms: a climate change co-stressor in marine and freshwater ecosystems. Harmful Algae 91:101590. https://doi.org/10.1016/j.hal.2019.03.008
Griffith AW, Shumway SE, Volety AK (2013) Bioaccumulation and depuration of brevetoxins in the eastern oyster (Crassostrea virginica) and the northern quahog (= hard clam, Mercenaria mercenaria). Toxicon 66:75–81. https://doi.org/10.1016/j.toxicon.2013.01.016
Guéguen M, Bardouil M, Baron R, Lassus P, Truquet P, Massardier J, Amzil Z (2008) Detoxification of pacific oyster Crassostrea gigas fed on diets of Skeletonema costatum with and without silt, following PSP contamination by Alexandrium minutum. Aquat Living Resour 21:13–20. https://doi.org/10.1051/alr:2008010
Guiry MD, Guiry GM (2016) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway http://www.algaebase.org
Gutiérrez JL, Jones CG, Strayer DL, Iribarne OO (2003) Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101:79–90. https://doi.org/10.1034/j.1600-0706.2003.12322.x
Haberkorn H, Lambert C, Le Goïc N, Guéguen M, Moal J, Palacios E, Lassus P, Soudant P (2010) Effects of Alexandrium minutum exposure upon physiological and hematological variables of diploid and triploid oysters, Crassostrea gigas. Aquat Toxicol 97:96–108. https://doi.org/10.1016/j.aquatox.2009.12.006
Haberkorn H, Tran D, Massabuau JC, Ciret P, Savar V, Soudant P (2011) Relationship between valve activity, microalgae concentration in the water and toxin accumulation in the digestive gland of the Pacific oyster Crassostrea gigas exposed to Alexandrium minutum. Mar Pollut Bull 62:1191–1197. https://doi.org/10.1016/j.marpolbul.2011.03.034
Hallegraeff GM (2010) Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge. J Phycol 46:220–235. https://doi.org/10.1111/j.1529-8817.2010.00815.x
Haubois AG, Bricelj VM, Naar J (2007) Transfer of brevetoxins to a Tellinid bivalve by suspension- and deposit-feeding and its implications for clay mitigation of Karenia brevis blooms. Mar Biol 151:2003–2012. https://doi.org/10.1007/s00227-007-0637-9
Hégaret H, Wikfors GH (2005a) 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 4:201–209. https://doi.org/10.1016/j.hal.2003.12.005
Hégaret H, Wikfors GH (2005b) Time-dependent changes in hemocytes of eastern oysters, Crassostrea virginica, and northern bay scallops, Argopecten irradians irradians, exposed to a cultured strain of Prorocentrum minimum. Harmful Algae 4:187–199. https://doi.org/10.1016/j.hal.2003.12.004
Hégaret H, Wikfors GH, Shumway SE (2007a) Diverse feeding responses of five species of bivalve mollusc when exposed to three species of harmful algae. J Shellfish Res 26:549–559. https://doi.org/10.2983/0730-8000(2007)26[549:DFROFS]2.0.CO;2
Hégaret H, da Silva PM, Wikfors GH, Lambert C, De Bettignies T, Shumway SE, Soudant P (2007b) Hemocyte responses of Manila clams, Ruditapes philippinarum, with varying parasite, Perkinsus olseni, severity to toxic-algal exposures. Aquat Toxicol 84:469–479. https://doi.org/10.1016/j.aquatox.2007.07.007
Hégaret H, Wikfors G, Soudant P, Lambert C, Shumway S, Bérard J, Lassus P (2007c) Toxic dinoflagellates (Alexandrium fundyense and A. catenella) have minimal apparent effects on oyster hemocytes. Mar Biol 152:441–447. https://doi.org/10.1007/s00227-007-0703-3
Hégaret H, Wikfors GH. Shumway SE (2009a) Biotoxin contamination and shellfish safety. In: Shumway SE, Rodrick GE (eds) Shellfish safety and quality. Woodhead Publishing Limited and CRC Press, pp 43-80.
Hégaret H, da Silva PM, Sunila I, Shumway SE, Dixon MS, Alix J, Wikfors GH, Soudant P (2009b) Perkinsosis in the Manila clam Ruditapes philippinarum affects responses to the harmful-alga, Prorocentrum minimum. J Exp Mar Biol Ecol 371:112–120. https://doi.org/10.1016/j.jembe.2009.01.016
Hégaret H, Smolowitz RM, Sunila I, Shumway SE, Alix J, Dixon M, Wikfors GH (2010) Combined effects of a parasite, QPX, and the harmful-alga, Prorocentrum minimum on northern quahogs, Mercenaria mercenaria. Mar Environ Res 69:337–344. https://doi.org/10.1016/j.marenvres.2009.12.008
Hégaret H, da Silva PM, Wikfors GH, Haberkorn H (2011) In vitro interactions between several species of harmful algae and haemocytes of bivalve molluscs. Cell Biol Toxicol 27:249–266. https://doi.org/10.1007/s10565-011-9186-6
Hégaret H, Brokordt KB, Gaymer CF, Lohrmann KB, García C, Varela D (2012) Effects of the toxic dinoflagellate Alexandrium catenella on histopathogical and escape responses of the Northern scallop Argopecten purpuratus. Harmful Algae 18:74–83. https://doi.org/10.1016/j.hal.2012.04.006
Hoagland P, Scatasta S (2006) The economic effects of harmful algal blooms. In: Granéli E, Turner J (eds) Ecology of harmful algae - ecological studies. Springer, Berlin, pp 391–419
Ianora A, Bentley MG, Caldwell GS, Casotti R, Cembella AD, Engström-öst J, Halsband C, Sonnenschein E (2011) The relevance of marine chemical ecology to plankton and ecosystem function: an emerging field. Mar Drugs 9:1625–1648. https://doi.org/10.3390/md9091625
Ibelings BW, Bruning K, De Jonge J, Wolfstein K, Pires LMD, Postma J, Burger T (2005) Distribution of microcystins in a lake foodweb: no evidence for biomagnification. Microb Ecol 49:487e500. https://doi.org/10.1007/s00248-004-0014-x
Ito K, Asakawa M, Beppu R, Takayama H, Miyazawa K (2004) PSP-toxicification of the carnivorous gastropod Rapana venosa inhabiting the estuary of Nikoh River, Hiroshima Bay, Hiroshima Prefecture, Japan. Mar Pollut Bull 48:1116–1121. https://doi.org/10.1016/j.marpolbul.2003.12.020
James KJ, Gillman M, Amandi MF, López-Rivera A, Puente PF, Lehane M, Mitrovic S, Furey A (2005) Amnesic shellfish poisoning toxins in bivalve molluscs in Ireland. Toxicon 46:852–858. https://doi.org/10.1016/j.toxicon.2005.02.009
James KJ, Carey B, O'Halloran J, Van Pelt FN, Skrabakova Z (2010) Shellfish toxicity: human health implications of marine algal toxins. Epidemiol Infect 138:927–940. https://doi.org/10.1017/S0950268810000853
Jauffrais T, Contreras A, Herrenknecht C, Truquet P, Séchet V, Tillmann U, Hess P (2012a) Effect of Azadinium spinosum on the feeding behaviour and azaspiracid accumulation of Mytilus edulis. Aquat Toxicol 124:179–187. https://doi.org/10.1016/j.aquatox.2012.08.016
Jauffrais T, Marcaillou C, Herrenknecht C, Truquet P, Séchet V, Nicolau E, Tillmann U, Hess P (2012b) Azaspiracid accumulation, detoxification and biotransformation in blue mussels (Mytilus edulis) experimentally fed Azadinium spinosum. Toxicon 60:582–595. https://doi.org/10.1016/j.toxicon.2012.04.351
Jiang TJ, Niu T, Xu YX (2006) Transfer and metabolism of paralytic shellfish poisoning from scallop (Chlamys nobilis) to spiny lobster (Panulirus stimpsoni). Toxicon 48:988–994. https://doi.org/10.1016/j.toxicon.2006.08.002
Jones TO, Whyte JNC, Ginther NG, Townsend LD, Iwama GK (1995) Haemocyte changes in the pacific oyster, Crassostrea gigas, caused by exposure to domoic acid in the diatom Pseudonitzschia pungens f. multiseries. Toxicon 33:347–353. https://doi.org/10.1016/0041-0101(94)00170-D
Kershaw DR (1983) Phylum Mollusca. In: Kershaw DR (ed) Animal diversity. Springer, Dordrecht, pp 169–191. https://doi.org/10.1007/978-94-011-6035-3_10
Khora SS, Jal S (2018) Occurrence of natural toxins in seafood. In: Holban AM, Grumezescu AM (eds), Microbial contamination and food degradation, Handbock of food bioengineering. Volume 10, Academic Press and Elsevier, pp 177-233. https://doi.org/10.1016/B978-0-12-811515-2/00007-X.
Kim JH, Lee KJ, Suzuki T, Mok JS, Park K, Kwon JY, Son KT, Song KC (2012) First report of contamination of the abalone Haliotis discus hannai by okadaic acid and yessotoxin. J Shellfish Res 3:1199–1203. https://doi.org/10.2983/035.031.0431
Kiørboe T, Møhlenberg F (1981) Particle selection in suspension-feeding bivalves. Mar Ecol Prog Ser 5:291–296
Kozlowsky-Suzuki B, Wilson AE, Ferrão-Filho ADS (2012) Biomagnification or biodilution of microcystins in aquatic foodwebs? Meta-analyses of laboratory and field studies. Harmful Algae 18:47–55. https://doi.org/10.1016/j.hal.2012.04.002
Kudela RM, Berdalet E, Bernard S, Burford M, Fernand L, Lu S, Roy S, Tester P, Usup G, Magnien R, Anderson DM, Cembella A, Chinain M, Hallegraef G, Reguera B, Zingone A, Enevoldsen H, Urban E (2015) Harmful algal blooms. In: A scientific summary for policy makers. IOC/UNESCO, Paris
Kvitek RG, DeGange AR, Beitler MK (1991) Paralytic shellfish poisoning toxins mediate feeding behavior of sea otters. Limnol Oceanogr 36:393–404. https://doi.org/10.4319/lo.1991.36.2.0393
Kwong RWM, Wang WX, Lam PKS, Yu PKN (2006) The uptake, distribution and elimination of paralytic shellfish toxins in mussels and fish exposed to toxic dinoflagellates. Aquat Toxicol 80:82–91. https://doi.org/10.1016/j.aquatox.2006.07.016
Landsberg JH (2002) The effects of harmful algal blooms on aquatic organisms. Rev Fish Sci 10:113–390. https://doi.org/10.1080/20026491051695
Lassudrie M, Soudant P, Richard G, Henry N, Medhioub W, da Silva PM, Donval A, Bunel M, Le Goïc N, Lambert C, de Montaudouin X, Fabioux C, Hégaret H (2014) Physiological responses of Manila clams Venerupis (=Ruditapes) philippinarum with varying parasite Perkinsus olseni burden to toxic algal Alexandrium ostenfeldii exposure. Aquat Toxicol 154:27–38. https://doi.org/10.1016/j.aquatox.2014.05.002
Lassudrie M, Wikfors GH, Sunila I, Alix JH, Dixon MS, Combot D, Soudant P, Fabioux C, Hégaret H (2015a) Physiological and pathological changes in the eastern oyster Crassostrea virginica infested with the trematode Bucephalus sp. and exposed to the toxic dinoflagellate Alexandrium fundyense. J Invertebr Pathol 126:51–63. https://doi.org/10.1016/j.jip.2015.01.011
Lassudrie M, Soudant P, Nicolas JL, Fabioux C, Lambert C, Miner P, Le Grand J, Petton B, Hégaret H (2015b) Interaction between toxic dinoflagellate Alexandrium catenella exposure and disease associated with herpesvirus OsHV-1μVar in Pacific oyster spat Crassostrea gigas. Harmful Algae 45:53–61. https://doi.org/10.1016/j.hal.2015.04.007
Lassudrie M, Hégaret H, Wikfors GH, da Silva PM (2020) Effects of marine harmful algal blooms on bivalve cellular immunity and infectious diseases: a review. Dev Comp Immunol 108:103660. https://doi.org/10.1016/j.dci.2020.103660
Lassus P, Fremy JM, Ledoux M, Bardouil M, Bohec M (1989) Patterns of experimental contamination by Protogonyaulax tamarensis in some French commercial shellfish. Toxicon 27:1313–1321. https://doi.org/10.1016/0041-0101(89)90063-9
Lassus P, Bardouil M, Baron R, Bérard J, Masselin P, Truquet P, Pitrat JP (2005) Improving detoxification efficiency of PSP-contaminated oysters (Crassostrea gigas Thunberg). Aquaculture Europe. http://archimer.ifremer.fr/doc/00000/2271/
Lassus P, Amzil Z, Baron R, Séchet V, Barillé L, Abadie E, Bardouil M, Sibat M, Truquet P, Bérard JB, Gueguen M (2007a) Modelling the accumulation of PSP toxins in Thau Lagoon oysters (Crassostrea gigas) from trials using mixed cultures of Alexandrium catenella and Thalassiosira weissflogii. Aquat Living Resour 20:59–67. https://doi.org/10.1051/alr:2007016
Lassus P, Gowland D, McKenzie D, Kelly M, Braaten B, Marcaillou-Martin C, Blanco J (2007b) Industrial scale detoxification of phycotoxin-contaminated shellfish: myth or reality? In: Busby P (ed) Proceedings of the sixth International Conference on Molluscan Shellfish Safety. The Royal Society of New Zealand, Blenheim, pp 289–297
Laurent D, Kerbrat AS, Darius HT, Rossi F, Yeeting B, Haddad M, Golubic S, Pauillac M, Chinain M (2012) Ciguatera shellfish poisoning (CSP): a new ecotoxicological phenomenon from cyanobacteria to humans via giant clams. In: Jensen MA, Muller DW (eds) Food chains. New Research, Nova Science, pp 1-43.
Le Goïc N, Hégaret H, Boulais M, Béguel JP, Lambert C, Fabioux C, Soudant P (2014) Flow cytometric assessment of morphology, viability, and production of reactive oxygen species of Crassostrea gigas oocytes. Application to Toxic dinoflagellate (Alexandrium minutum) exposure. Cytometry A 85:1049–1056. https://doi.org/10.1002/cyto.a.22577
Lopes VM, Baptista M, Repolho T, Rosa R, Costa PR (2014) Uptake, transfer and elimination kinetics of paralytic shellfish toxins in common octopus (Octopus vulgaris). Aquat Toxicol 146:205–211. https://doi.org/10.1016/j.aquatox.2013.11.011
Lopes VM, Costa PR, Rosa R (2019) Effects of harmful algal bloom toxins on marine organisms. In: Duarte B, Caçador I (eds) Ecotoxicology of marine organisms. CRC Press, Boca Raton, p 47. https://doi.org/10.1201/b22000
López-Rivera A, O’Callaghan K, Moriarty M, O’Driscoll D, Hamilton B, Lehane M, James KJ, Furey A (2010) First evidence of azaspiracids (AZAs): a family of lipophilic polyether marine toxins in scallops (Argopecten purpuratus) and mussels (Mytilus chilensis) collected in two regions of Chile. Toxicon 55:692–701. https://doi.org/10.1016/j.toxicon.2009.10.020
MacKenzie L, Beuzenberg V, Holland P, McNabb P, Selwood A (2004) Solid phase adsorption toxin tracking (SPATT): a new monitoring tool that simulates the biotoxin contamination of filter feeding bivalves. Toxicon 44:901–918. https://doi.org/10.1016/j.toxicon.2004.08.020
MacQuerrie SP, Bricelj VM (2008) Behavioral and physiological responses to PSP toxins in Mya arenaria populations in relation to previous exposure to red tides. Mar Ecol Prog Ser 366:59–74. https://doi.org/10.3354/meps07538
Mafra LL Jr, Bricelj VM, Ouellette C, Léger C, Bates SS (2009) Mechanisms contributing to low domoic acid uptake by oysters feeding on Pseudo-nitzschia cells. I. Filtration and pseudofeces production. Aquat Biol 6:201–212. https://doi.org/10.3354/ab00121
Mafra LL Jr, Bricelj VM, Ouellette C, Bates SS (2010) Feeding mechanics as the basis for differential uptake of the neurotoxin domoic acid by oysters, Crassostrea virginica, and mussels, Mytilus edulis. Aquat Toxicol 97:160–171. https://doi.org/10.1016/j.aquatox.2010.01.009
Mafra LL Jr, Ribas T, Alves TP, Proença LAO, Schramm MA, Uchida H, Suzuki T (2015) Differential okadaic acid accumulation and detoxification by oysters and mussels during natural and simulated Dinophysis blooms. Fish Sci 81:749–762. https://doi.org/10.1007/s12562-015-0882-7
Mafra LL Jr, Nolli PKW, Mota LE, Domit C, Soeth M, Luz LFG, Sobrinho BF, Leal JG, Di Domenico M (2019) Multi-species okadaic acid contamination and human poisoning during a massive bloom of Dinophysis acuminata complex in southern Brazil. Harmful Algae 89:101662. https://doi.org/10.1016/j.hal.2019.101662
Magdalena AB, Lehane M, Krys S, Fernández ML, Furey A, James KJ (2003) The first identification of azaspiracids in shellfish from France and Spain. Toxicon 42:105–108. https://doi.org/10.1016/s0041-0101(03)00105-3
Mat AM, Haberkorn H, Bourdineaud JP, Massabuau JC, Tran D (2013) Genetic and genotoxic impacts in the oyster Crassostrea gigas exposed to the harmful alga Alexandrium minutum. Aquat Toxicol 140-141:458–465. https://doi.org/10.1016/j.aquatox.2013.07.008
Matsuyama Y, Uchida T, Honjo T (1997) Toxic effects of the dinoflagellate Heterocapsa circularisquama on clearance rate of the blue mussel Mytilus galloprovincialis. Mar Ecol Prog Ser 146:73–80
May SP, Burkholder JM, Shumway SE, Hégaret H, Wikfors GH, Frank D (2010) Effects of the toxic dinoflagellate Alexandrium monilatum on survival, grazing and behavioral response of three ecologically important bivalve molluscs. Harmful Algae 9:281–293. https://doi.org/10.1016/j.hal.2009.11.005
Medhioub W, Ramondenc S, Vanhove AS, Vergnes A, Masseret E, Savar V, Amzil Z, Laabir M, Rolland JL (2013) Exposure to the neurotoxic dinoflagellate, Alexandrium catenella, induces apoptosis of the hemocytes of the oyster Crassostrea gigas. Mar Drugs 11:4799–4814. https://doi.org/10.3390/md11124799
Mello DF, Proença LAO, Barracco MA (2010) Comparative study of various immune parameters in three bivalve species during a natural bloom of Dinophysis acuminata in Santa Catarina Island, Brazil. Toxins 2:1166–1178. https://doi.org/10.3390/toxins2051166
Miller MA, Kudela RM, Mekebri A, Crane D, Oates SC, Tinker MT, Staedler M, Miller WA, Toy-Choutka S, Dominik C, Hardin D, Langlois G, Murray M, War K, Jessup DA (2010) Evidence for a novel marine harmful algal bloom: cyanotoxin (microcystin) transfer from land to sea otters. PLoS One 5:e12576. https://doi.org/10.1371/journal.pone.0012576
Molinet C, Niklitschek E, Seguel M, Díaz P (2010) Trends of natural accumulation and detoxification of paralytic shellfish poisoning in two bivalves from the Northwest Patagonian inland sea. Rev Biol Mar Oceanogr 45:195–204. https://doi.org/10.4067/S0718-19572010000200001
Monteiro A, Costa PR (2011) Distribution and selective elimination of paralytic shellfish toxins in different tissues of Octopus vulgaris. Harmful Algae 10:732–737. https://doi.org/10.1016/j.hal.2011.06.004
Montojo UM, Sakamoto S, Cayme MF, Gatdula NC, Furio EF, Relox JR Jr, Shigeru S, Fukuyo Y, Kodama M (2006) Remarkable difference in accumulation of paralytic shellfish poisoning toxins among bivalve species exposed to Pyrodinium bahamense var. compressum bloom in Masinloc bay, Philippines. Toxicon 48:85–92. https://doi.org/10.1016/j.toxicon.2006.04.014
Mu C, Li Q (2013) Effects of the dinoflagellate Alexandrium catenella on the early development of the Pacific oyster Crassostrea gigas. J Shellfish Res 32:689–694. https://doi.org/10.2983/035.032.0310
Murray SA, O'Connor WA, Alvin A, Mihali TK, Kalaitzis J, Neilan BA (2009) Differential accumulation of paralytic shellfish toxins from Alexandrium minutum in the pearl oyster, Pinctada imbricata. Toxicon 54:217–223. https://doi.org/10.1016/j.toxicon.2009.04.005
Neves RAF, Rodrigues ET (2020) Harmful algal blooms: effect on coastal marine ecosystems. In: Azul AM, Brandli L, Leal Filho W, Özuyar PG., Wall T (eds) Encyclopedia of the UN Sustainable Development Goals. Life Below Water. Springer Internacional Publishing
Neves RAF, Valentin JL, Figueiredo GM, Hégaret H (2015a) Responses of the common periwinkle Littorina littorea to exposure to the toxic dinoflagellate Alexandrium minutum. J Molluscan Stud 81:308–311. https://doi.org/10.1093/mollus/eyu092
Neves RAF, Figueiredo GM, Valentin JL, Da Silva PM, Hégaret H (2015b) Immunological and physiological responses of the periwinkle Littorina littorea during and after exposure to the toxic dinoflagellate Alexandrium minutum. Aquat Toxicol 160:96–105. https://doi.org/10.1016/j.aquatox.2015.01.010
Neves RAF, Santiago TC, Carvalho WF, Silva ES, da Silva PM, Nascimento SM (2019) Impacts of the toxic benthic dinoflagellate Prorocentrum lima on the brown mussel Perna perna: Shell-valve closure response, immunology, and histopathology. Mar Environ Res 146:35–45. https://doi.org/10.1016/j.marenvres.2019.03.006
Neves RAF, Naveira C, Miyahira IC, Portugal SGM, Krepsky N, Santos LN (2020) Are invasive species always negative to aquatic ecosystem services? The role of dark false mussel for water quality improvement in a multi-impacted urban coastal lagoon. Water Res 184:116108. https://doi.org/10.1016/j.watres.2020.116108
Nicolas J, Hoogenboom RLAP, Hendriksen PJM, Bodero M, Bovee TFH, Rietjens IMCM, Gerssen A (2017) Marine biotoxins and associated outbreaks following seafood consumption: prevention and surveillance in the 21st century. Glob Food Sec 15:11–21. https://doi.org/10.1016/j.gfs.2017.03.002
Núñez-Acuña G, Aballay AE, Hégaret H, Astuya AP, Gallardo-Escárate C (2013) Transcriptional responses of Mytilus chilensis exposed in vivo to saxitoxin (STX). J Molluscan Stud 79:323–331. https://doi.org/10.1093/mollus/eyt030
O’Mahony M (2018) Eu regulatory risk management of marine biotoxins in the marine bivalve mollusc food-chain. Toxins 10:118. https://doi.org/10.3390/toxins10030118
Oikawa H, Fujita T, Saito K, Watabe S, Satomi M, Yano Y (2004) Comparison of paralytic shellfish poisoning toxin between carnivorous crabs (Telmessus acutidens and Charybdis japonica) and their prey mussel (Mytilus galloprovincialis) in an inshore food chain. Toxicon 43:713–719. https://doi.org/10.1016/j.toxicon.2004.03.003
Persson A, Smith BC (2009) Consumption of Scrippsiella lachrymosa resting cysts by the eastern oyster (Crassostrea virginica). J Shellfish Res 28:221–225. https://doi.org/10.2983/035.028.0227
Persson A, Smith BC, Wikfors GH, Quilliam M (2006) Grazing on toxic Alexandrium fundyense resting cysts and vegetative cells by the eastern oyster (Crassostrea virginica). Harmful Algae 5:678–684. https://doi.org/10.1016/j.hal.2006.02.004
Persson A, Smith BC, Dixon MS, Wikfors GH (2008) The eastern mudsnail, Ilyanassa obsoleta, actively forages for, consumes, and digests cysts of the dinoflagellate, Scrippsiella lachrymosa. Malacologia 50:341–345. https://doi.org/10.4002/0076-2997-50.1-2.341
Ritchie H, Roser M (2019) Seafood Production. http://ourworldindata.org/seafood-production
Robertson A, Stirling D, Robillot C, Llewellyn L, Negri A (2004) First report of saxitoxin in octopi. Toxicon 44:765–771. https://doi.org/10.1016/j.toxicon.2004.08.015
Rolland JL, Pelletier K, Masseret E, Rieuvilleneuve F, Savar V, Santini A, Amzil Z, Laabir M (2012) Paralytic toxins accumulation and tissue expression of α-amylase and lipase genes in the pacific oyster Crassostrea gigas fed with the neurotoxic dinoflagellate Alexandrium catenella. Mar Drugs 10:2519–2534. https://doi.org/10.3390/md10112519
Rolland JL, Medhioub W, Vergnes A, Abi-Khalil C, Savar V, Abadie E, Masseret E, Amzil Z, Laabir M (2014) A feedback mechanism to control apoptosis occurs in the digestive gland of the oyster Crassostrea gigas exposed to the paralytic shellfish toxins producer Alexandrium catenella. Mar Drugs 12:5035–5054. https://doi.org/10.3390/md12095035
Rolton A, Vignier J, Soudant P, Shumway SE, Bricelj VM, Volety AK (2014) Effects of the red tide dinoflagellate, Karenia brevis, on early development of the eastern oyster Crassostrea virginica and northern quahog Mercenaria mercenaria. Aquat Toxicol 155:199–206. https://doi.org/10.1016/j.aquatox.2014.06.023
Rolton A, Soudant P, Vignier J, Pierce R, Henry M, Shumway SE, Bricelj VM, Volety AK (2015) Susceptibility of gametes and embryos of the eastern oyster, Crassostrea virginica, to Karenia brevis and its toxins. Toxicon 99:6–15. https://doi.org/10.1016/j.toxicon.2015.03.002
Romero-Geraldo RDJ, García-Lagunas N, Hernández-Saavedra NY (2014) Effects of in vitro exposure to diarrheic toxin producer Prorocentrum lima on gene expressions related to cell cycle regulation and immune response in Crassostrea gigas. PLoS One 9:e97181. https://doi.org/10.1371/journal.pone.0097181
Roué M, Darius HT, Picot S, Ung A, Viallon J, Gaertner-Mazouni N, Sibat M, Amzil Z, Chinain M (2016) Evidence of the bioaccumulation of ciguatoxins in giant clams (Tridacna maxima) exposed to Gambierdiscus spp. cells. Harmful Algae 57:78–87. https://doi.org/10.1016/j.hal.2016.05.007
Roué M, Darius H, Ung A, Viallon J, Sibat M, Hess P, Amzil Z, Chinain M (2018) Tissue distribution and elimination of ciguatoxins in Tridacna maxima (Tridacnidae, Bivalvia) fed Gambierdiscus polynesiensis. Toxins 10:189. https://doi.org/10.3390/toxins10050189
Schramm MA, Tamanaha MS, Beirão LH, Proença LA (2006) Toxinas paralisantes em mexilhão Perna perna em áreas de cultivo da costa sul do Brasil: estudo de caso. Braz J Food Nutr 17:443–450
Sephton DH, Haya K, Martin JL, Legresley MM, Page FH (2007) Paralytic shellfish toxins in zooplankton, mussels, lobsters and caged Atlantic salmon, Salmo salar, during a bloom of Alexandrium fundyense off Grand Manan Island, in the Bay of Fundy. Harmful Algae 6:745–758. https://doi.org/10.1016/j.hal.2007.03.002
Shumway SE (1990) A review of the effects of algal blooms on shellfish and aquaculture. J World Aquacult Soc 21:65–104. https://doi.org/10.1111/j.1749-7345.1990.tb00529.x
Shumway SE (1995) Phycotoxin-related shellfish poisoning: bivalve molluscs are not the only vectors. Rev Fish Sci 3:1–31. https://doi.org/10.1080/10641269509388565
Shumway SE, Cucci TL (1987) The effects of the toxic dinoflagellate Protogonyaulax tamarensis on the feeding and behaviour of bivalve molluscs. Aquat Toxicol 10:9–27. https://doi.org/10.1016/0166-445X(87)90024-5
Shumway SE, Gainey LF Jr (1992) A review of physiological effects of toxic dinoflagellates on bivalve molluscs. In: Gittenberger E, Goud J (eds) Proceedings of Ninth International Malacological Congress. Unitas Malacologica, Leiden, pp 357–362
Shumway SE, van Egmond HP, Hurst JW, Bean LL (1995) Management of shellfish resources. In: Hallegraeff GM, Anderson DM, Cembella AD (eds) Manual of Harmful Marine Microalgae. IOC Manuals and Guides vol. 33, UNESCO, pp 436-463.
Shumway SE, Allen SM, Dee Boersma P (2003) Marine birds and harmful algal blooms: sporadic victims or under-reported events? Harmful Algae 2:1–17. https://doi.org/10.1016/S1568-9883(03)00002-7
Shumway SE, Burkholder JM, Springer J (2006) Effects of the estuarine dinoflagellate Pfiesteria shumwayae (Dinophyceae) on survival and grazing activity of several shellfish species. Harmful Algae 5:442–458. https://doi.org/10.1016/j.hal.2006.04.013
Silvert W, Bricelj M, Cembella A (1998) Dynamic modelling of PSP toxicity in the surfclam (Spisula solidissima): multicompartimental kinetics and biotransformation. In: Reguera B, Blanco J, Fernández ML, Wyatt T (eds) Harmful Algae. Xunta de Galicia and IOC of UNESCO, Santiago de Compostela, pp 437–440
Smolowitz R, Shumway SE (1997) Possible cytotoxic effects of the dinoflagellate, Gyrodinium aureolum, on juvenile bivalve molluscs. Aquac Int 5:291–300. https://doi.org/10.1023/A:1018355905598
Sokolova IM, Sukhotin AA, Lannig G (2011) Stress effects on metabolism and energy budgets in mollusks. In: Abele D, Vázquez-Medina JP, Zenteno-Savín T (eds) Oxidative Stress in Aquatic Ecosystems. John Wiley & Sons, Chichester, pp 261–280
Sotton BT, Guillard J, Anneville O, Maréchal M, Savichtcheva O, Domaizon I (2014) Trophic transfer of microcystins through the lake pelagic food web: evidence for the role of zooplankton as a vector in fish contamination. Sci Total Environ 466-467:152–163. https://doi.org/10.1016/j.scitotenv.2013.07.020
Soudant P, Chu FLE, Volety A (2013) Host-parasite interactions: marine bivalve molluscs and protozoan parasites, Perkinsus species. J Invertebr Pathol 114:196–216. https://doi.org/10.1016/j.jip.2013.06.001
Springer JJ, Shumway SE, Burkholder JM, Glasgow HB (2002) Interactions between the toxic estuarine dinoflagellate Pfiesteria piscicida and two species of bivalve molluscs. Mar Ecol Prog Ser 245:1–10. https://doi.org/10.3354/meps245001
Stobo LA, Lacaze JPCL, Scott AC, Petrie J, Turrell EA (2008) Surveillance of algal toxins in shellfish from Scottish waters. Toxicon 51:635–648. https://doi.org/10.1016/j.toxicon.2007.11.020
Suzuki T, Mitsuya T (2001) Comparison of dinophysistoxin-1 and esterified dinophysistoxin-1 (dinophysistoxin-3) contents in the scallop Patinopecten yessoensis and the mussel Mytilus galloprovincialis. Toxicon 39:905–908. https://doi.org/10.1016/s0041-0101(00)00205-1
Suzuki T, Ichimi K, Oshima Y, Kamiyama T (2003) Paralytic shellfish poisoning (PSP) toxin profiles and short-term detoxification kinetics in mussels Mytilus galloprovincialis fed with the toxic dinoflagellate Alexandrium tamarense. Harmful Algae 2:201–206. https://doi.org/10.1016/S1568-9883(03)00042-8
Talmage SC, Gobler CJ (2012) Effects of CO2 and the harmful alga Aureococcus anophagefferens on growth and survival of oyster and scallop larvae. Mar Ecol Prog Ser 464:121–134. https://doi.org/10.3354/meps09867
Tran D, Haberkorn H, Soudant P, Ciret P, Massabuau JC (2010) Behavioral responses of Crassostrea gigas exposed to the harmful algae Alexandrium minutum. Aquaculture 298:338–345. https://doi.org/10.1016/j.aquaculture.2009.10.030
Tran D, Ciutat A, Mat A, Massabuau JC, Hégaret H, Lambert C, Le Goïc N, Soudant P (2015) The toxic dinoflagellate Alexandrium minutum disrupts daily rhythmic activities at gene transcription, physiological and behavioral levels in the oyster Crassostrea gigas. Aquat Toxicol 158:41–49. https://doi.org/10.1016/j.aquatox.2014.10.023
Turner AD, Lewis AM, Bradley K, Maskrey BH (2021) Marine invertebrate interactions with harmful algal blooms –iImplications for one health. J Invertebr Pathol:107555. https://doi.org/10.1016/j.jip.2021.107555.
Twarog BM (1974) “Immunity” to paralytic shellfish toxin in bivalve molluscs. In: Cameron AM (ed) Proceedings of the Second International Coral Reef Symposium. Great Barrier Reef Committee, Brisbane, pp 505–512
Twarog BM, Yamaguchi H (1975) Resistance to paralytic shellfish toxins in bivalve molluscs. In: Lo Cicero VR (ed) Proceedings of the First International Conference on Toxic Dinoflagellate Blooms. Mass Science and Technology Foundation, Wakefield, pp 381–393
Twarog BM, Hidaka T, Yamaguchi H (1972) Resistance to tetrodotoxin and saxitoxin in nerves of bivalve molluscs. Toxicon 10:273–278. https://doi.org/10.1016/0041-0101(72)90012-8
Vale P, Sampayo MAM (2001) Domoic acid in Portuguese shellfish and fish. Toxicon 39:893–904. https://doi.org/10.1016/S0041-0101(00)00229-4
Van Dolah FM (2000) Marine algal toxins: origins, health effects, and their increased occurrence. Environ Health Perspect 108:133–141. https://doi.org/10.1289/ehp.00108s1133
Wekell JC, Lorenzana RM, Hogan M, Barnett H (1996) Survey of paralytic shellfish poison and domoic acid in Puget Sound predatory gastropods. J Shellfish Res 15:231–236
Wells ML, Trainer VL, Smayda TJ, Karlson BSO, Trick CG, Kudela RM, Ishikawa A, Bernard S, Wulff A, Anderson DM, Cochlan WP (2015) Harmful algal blooms and climate change: learning from the past and present to forecast the future. Harmful Algae 49:68–93. https://doi.org/10.1016/j.hal.2015.07.009
Wikfors GH, Smolowitz RM (1995) Experimental and histological studies of four life-history stages of the eastern oyster, Crassostrea virginica, exposed to a cultured strain of the dinoflagellate Prorocentrum minimum. Biol Bull 188:313–328. https://doi.org/10.2307/1542308
Wohlgeschaffen GD, Mann KH, Subba Rao DV, Pocklington R (1992) Dynamics of the phycotoxin domoic acid: accumulation and excretion in two commercially important bivalves. J Appl Phycol 4:297–310. https://doi.org/10.1007/BF02185786
Xiao X, Agustí S, Pan Y, Yu Y, Li K, Wu J, Duarte CM (2019) Warming amplifies the frequency of harmful algal blooms with eutrophication in Chinese coastal waters. Environ Sci Technol 53:13031–13041. https://doi.org/10.1021/acs.est.9b03726
Yee-Duarte JA, Ceballos-Vázquez BP, Arellano-Martínez M, Camacho-Mondragón MA, Uría-Galicia E (2018) Histopathological alterations in the gonad of Megapitaria squalida (Mollusca: Bivalvia) inhabiting a heavy metals polluted environment. J Aquat Anim Health 30:144–154. https://doi.org/10.1002/aah.10015
Zohdi E, Abbaspour M (2019) Harmful algal blooms (red tide): a review of causes, impacts and approaches to monitoring and prediction. Int J Environ Sci Technol 16:1789–1806. https://doi.org/10.1007/s13762-018-2108-x
Acknowledgements
Authors are grateful to Geovanna Theobald Borsato and Rodrigo Almeida F. da Silva for some of the microalga figures (used in Fig. 2) and to anonymous reviewers that contributed for manuscript improvement.
Funding
This study was financially supported by Foundation Carlos Chagas Filho Research Support of the State of Rio de Janeiro (FAPERJ) through Research Grants attributed to LNS (E-26/202.840/2015; E-26/202.755/2018), by The Brazilian National Council for Scientific and Technological Development (CNPq) through Research Grants attributed to LNS (312194/2015-3; 314379/2018-5), and by the Federal University of the State of Rio de Janeiro (UNIRIO) – [INOVA UNIRIO IN-01/2019] attributed to RAFN.
Author information
Authors and Affiliations
Contributions
Conceptualization: RAFN, SMN, LNS; Methodology: RAFN, LNS; Validation: RAFN; Formal analysis: RAFN; Investigation: RAFN; Writing – Original draft: RAFN, SMN, LNS; Writing- Review & editing: RAFN, SMN, LNS; Visualization: RAFN, SMN, LNS.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable
Consent for publication
Not applicable
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Vitor Vasconcelos
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
ESM 1
(DOC 476 kb)
Rights and permissions
About this article
Cite this article
Neves, .A.F., Nascimento, S.M. & Santos, L.N. Harmful algal blooms and shellfish in the marine environment: an overview of the main molluscan responses, toxin dynamics, and risks for human health. Environ Sci Pollut Res 28, 55846–55868 (2021). https://doi.org/10.1007/s11356-021-16256-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-16256-5