Effects of Harmful Algal Blooms on Fish and Shellfish Species: A Case Study of New Zealand in a Changing Environment

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Effects of Harmful Algal Blooms on Fish and Shellfish Species: A Case Study of New Zealand in a Changing Environment



1. Introduction

New Zealand Aquaculture and HABs

2. Effects of Bloom Forming HAB Species on Species of Relevance to the NZ Aquaculture Industry

2.1. Alexandrium and Gymnodinium spp.

2.2. Karenia spp.

2.3. Dinophysis spp.

2.4. Pseudo-nitzschia spp.

2.5. The Raphidophytes: Heterosigma and Fibrocapsa

2.6. Other Bloom Forming HAB Species in New Zealand

3. Future Issues

3.1. Ichthyotoxic HAB Species Present in New Zealand

3.1.1. Potentially Harmful Taxa Detected Using High-Throughput Sequencing Metabarcoding

3.2. HABs in a Changing Environment

4. Conclusions and Future Directions

5. Materials and Methods

5.1. Sampling, PCR Conditions and High-Throughput Sequencing

5.2. Amplicon Sequence Variant Inference and Taxonomic Assignments

Supplementary Materials

Author Contributions


Institutional Review Board Statement

Informed Consent Statement

Data Availability Statement


Conflicts of Interest


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Class Genus Species # Effects on Shellfish and Fish Exposure to Key References
Bacillariophyceae Pseudo-nitzschia Larvae of Pecten maxiumus: growth, development and survival reduced Domoic Acid (DA) [46]
P. australis (DA-producer)

P. fraudulenta (DA-producer)

Juvenile P. maximus & Crassostrea gigas: Preferential filtration of non-toxic algae

C.g.: Reduction in clearance rate (P. australis only)

Whole cell culture [47]
P. multiseries (DA-producer) Juvenile & adult C. virginica: increased pseudofaeces production, lower filtration rates Whole cell culture [48,49,50]
C.v. & Mytilus edulis: selective rejection of toxic cells Whole cell culture [51]
M.e.: no effect on larval survival & development but, increased phenoloxidase production Whole cell culture & DA [52]
Adult C. gigas: Reduction in the number and phagocytic activity of hemocytes Whole cell culture [53]
P. delicatissima (non-toxic) Adult C.v.: lower filtration rate Whole cell culture [50]
Juvenile sea bass (Dicentrarchus labrax): mucus over production in gills Whole cell culture [54]
Dictyophyceae Pseudochattonella P. verruculosa (Hara & Chihara) Mortality of sea-cage salmon, Oncorhynchus tshawytscha Field bloom [43]
Dinophyceae Alexandrium Adult and larvae of various fish spp.: mortalities and impairment of sensory-motor function Field blooms, whole cell culture, paralytic shellfish toxins & saxitoxins [19] (and references there in)
Alexandrium pacificum Adult Perna canaliculus: Reduction in byssus production, reversable temporary increase in oxygen uptake Whole cell culture [55,56] (as A. tamarense)
P.c. spat (2 mm): Reduction in byssal pad production and growth Whole cell culture [57]
Adult Pecten novaezelandiae: clearance rate reduced and altered in other bivalve species. Whole cell culture [58,59]

(as A. tamarense)

Adult Argopecten irradians, Geukensia demissa, Mercenaria mercenaria, Mya arenaria, Mytilus edulis, Ostrea edulis, Paphies donacina, Placopecten magellanicus and Spisula solidissima: various effects including shell valve closure, changes in clearance rate, production of mucus, inhibition of byssus production, violent swimming & erratic siphon activity Whole cell culture [34,55,60,61,62]

(as Gonyaulax tamarensis, Protogonyaulax tamarensis and A. tamarense)

Juvenile C. gigas: changes in hemocyte parameters Whole cell culture [63] (as A. catenella)
A. irradians larvae: increased mortalities; reduced activity, and growth of larvae; reduced attachment and climbing ability of juveniles Whole cell culture & saxitoxin [64,65]

(as A. tamarense, strain ATHK)

Alexandrium minutum Adult C. gigas: reduced clearance and filtration rate, increased shell micro-closures, inflammatory response in digestive gland, increased circulating hemocyte concentration and phagocytic ability, genotoxic effects and increased detoxification/antioxidant gene expression. Reduced motility and ATP content of sperm, smaller larval size and increased mortalities at settlement Whole cell culture [66,67,68,69,70,71,72,73]
Gametes and larvae of C.g.: increased ROS in oocytes, decrease in sperm viability & fertilization. Reduced larval hatching, swimming, feeding, growth, settlement and survival Whole cell culture [16,17,74]
Adult P. maximus: delayed shell growth, alteration of sensing processes, less efficient escape response, muscular damage Whole cell culture [75]
Cerataulina pelagica C. pelagica Mortality of Fin fish & shellfish Field bloom (lack of oxygen) [76]
Gonyaulax Gonyaulax fragilis Mortality of marine fauna including fin-fish. Field bloom (slime) [77]
Dinophysis Lethal and sub-lethal effects on various fin fish species, including: behavioural changes, poor co-ordination, inactivity, oxidative stress and histological changes in adults, and: reduced hatching, swimming activity, growth & feeding of larvae Okadaic Acid & dinophysis toxins [18] (and references there in)
Dinophysis acuminata Adult C. gigas, Perna perna & Anomalocardia brasiliana: Changes in the hemocyte immunological parameters, especially in P. perna. Hemocyte infiltration in the digestive gland of C. gigas. Field bloom [78,79]
Gametes of C.g.: increased oocyte mortality & reduced fertilization success Whole cell culture [80]
Gymnodinium Gymnodinium catenatum Mortality of finfish Field blooms [81,82]
C. gigas spat (3 mm): reduced clearance rate, increased valve closure & pseudofaeces production. Inflammation of the gill and digestive gland Whole cell culture [83,84]
C.g. larvae: no observable effects Whole cell culture [85]
Juvenile Argopecten ventricosus & Nodipecten subnodosus Whole cell culture [86,87,88]
Karenia K. brevisulcatum (Chang) Gert Hansen & Moestrup Mortalities of fish and shellfish Field blooms [89,90]
Mortality of various larval & juvenile fish and shellfish species (Oncorhynchus tschawytscha, Chrysophrys auratus, P. canaliculus, Evechinus chloroticus and Haliotis iris, Pleurobranchia maculata, C. gigas) Whole cell culture, cell free culture, SPE extract, purified brevisulcatic acids [91]
K. mikimotoi (Miyake & Kominami ex Oda) Gert Hansen & Moestrup Fish (Sciaenops ocellatus) erythrocytes: hemolytic activity Crude algal extract [92]
Lethal and sublethal effects on finfish and shellfish Field blooms, whole cell culture [23,93,94,95] (and references there in)
Fin fish, eel and abalone mortalities Field blooms [96,97,98]
Various adult shellfish species: reduced clearance rates, changes in immune functions, reduced escape locomotion and paralysis Field blooms, whole cell culture [33,61,93,99,100,101,102,103,104] (as Gyrodinium aureolum)
Various larval shellfish species: embryo, larval and spat mortalities, reduction in activity rate Whole cell culture, SPE extract, bloom water, filtered bloom water [85,91,105,106,107,108,109]
K. sellifomis Haywood, Steidinger & MacKenzie Mortality of various fin fish & shellfish, especially Haliotis iris, Paphies subtriangulata & P. canaliculus Field bloom [110,111]
Mortality of various fin fish & shellfish Field bloom [112,113] (references there in)
C. gigas larvae: mortalities Whole cell culture [114]
Adult Ruditapes philippinarum: hemocyte variables changed Whole cell culture [103,115]
K. umbella de Salas, Bolch & Hallegraeff Mortalities of Oncorhynchus mykiss & Salmo salar Field bloom [116]
Ostreopsis O. cf. siamensis Mortalities of sea urchins, Evechinus chloroticus Field bloom [117,118]
Haptophyceae Prymnesium P. calathiferum Chang & Ryan Fish and shellfish mortalities Field bloom [119]
Raphidophyceae Heterosigma H. akashiwo (Hada) Sournia Mortality of O. tschawytscha Field bloom [41,120]
Mortalities of various juvenile and adult fin fish Field blooms, toxins from blooms [94,121,122,123]
Pinctada fucata martensii & Argopecten irradians gametes & larvae: Reduced sperm swimming velocity, increased mortalities & abnormalities, reduced activity of trocophore & D-larvae Cell free culture, whole cell culture [124,125,126]
Adult C. virginica: shell closure, reduction in filtration and increased hepatopancreas lysosomal destabilization Whole cell culture [32,127]
C. virginica and M. mercenaria hemocytes (in vitro): mortality Whole cell culture, culture filtrate [33]
Fibrocapsa F. japonica Adult C. virginica: increased lysosomal destabilization in digestive gland Bloom water [128]
Solea solea larvae: mortality Whole cell culture, culture extracts [129]
Class Genus Species # Effects on Shellfish and Fish Exposure to Key References
Dinophyceae Alexandrium A. ostenfeldii Adult Ruditapes philippinarum & C. gigas: tissue inflammatory response, changes in hemocyte morphology, oxidative stress response in the gills Whole cell culture [173,174]
Cochlodinium (=Margalefidinium) C. polykrikoides Mortalities of finfish Field blooms [94,175]
Adult Argopecten irradians, C. gigas, M. mercenaria: mortalities and reduced growth Field blooms [176] (and references there in)
Juvenile A. irradians and Cyprinodon variegates: mortalities Whole cell culture, cell free culture medium [177]
Heterocapsa H. cf. circularisquama Horiguchi Pinctada fucata, C. gigas, M. galloprovincialis, Venerupis philippinarum, Suculus diversicolor: Adults: Mortalities, reduced filtration rate. Larvae: activity rate, development rate and survival reduced Field blooms, bloom water, whole cell culture [29,85,178,179,180]
H. illdefina (Herman & Sweeney) Morrill & Loeblich III None known [114,181]
Karlodinium K. veneficum (Ballentine) Larsen Fin fish mortalities Field bloom, whole cell culture, cell lysate [182,183,184]
C. virginica & C. ariakensis larvae, spat & juveniles: increased mortalities & abnormalities, reduction in swimming and activity, reduced growth rates. Whole cell culture [185,186,187,188,189]
Juvenile & adult Mytilus edulis & Mercenaria mercenaria: increased hemocyte phagocytosis and ROS production, reduced growth rates Whole cell culture [188,190]
Pfiesteria Pfiesteria spp. Fin fish mortalities Field blooms [191,192]
P. piscicida Steidinger & Burkholder A. irradians, C. gigas & C. virginica larvae: mortalities Whole cells [193,194]
P. shumwayae Glasgow & Burkholder (syn. Pseudopfiesteria shumwayae (Glasgow & Burkholder)) Ichthyotoxic in vitro Whole cell culture [195]
A. irradians, C. virginica, M. mercenaria, Perna viridis: mortalities of larvae & adults Whole cell culture [196]
Prorocentrum P. rathymum Loeblich, Shirley & Schmidt C. gigas spat: mortality Methanol extracts [197]
Haptophyceae Chrysochromulina C. leadbeateri Estep, Davis, Hargreaves & Sieburth Mortalities of Salmo salar Field bloom [27,198]
Pavlomulina P. ranunculiformis Sym, Pienaar & Kawachi Attaching to C. gigas larvae whole cell culture [28]
Raphidophyceae Chattonella C. antiqua (Hada) Ono (syn.

C. marina var. antiqua (Hada) Demura & Kawachi)

Fin fish mortalities Field bloom [94,199]
Mortalities Thunnus maccoyii Field bloom [200,201]
Pinctada fucata martensii: reduced sperm swimming velocity, increased larval mortalities & abnormalities, reduced activity Whole cell culture [124,125]

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Rolton, A.; Rhodes, L.; Hutson, K.S.; Biessy, L.; Bui, T.; MacKenzie, L.; Symonds, J.E.; Smith, K.F. Effects of Harmful Algal Blooms on Fish and Shellfish Species: A Case Study of New Zealand in a Changing Environment. Toxins 2022, 14, 341. https://doi.org/10.3390/toxins14050341

Rolton A, Rhodes L, Hutson KS, Biessy L, Bui T, MacKenzie L, Symonds JE, Smith KF. Effects of Harmful Algal Blooms on Fish and Shellfish Species: A Case Study of New Zealand in a Changing Environment. Toxins. 2022; 14(5):341. https://doi.org/10.3390/toxins14050341

Chicago/Turabian Style

Rolton, Anne, Lesley Rhodes, Kate S. Hutson, Laura Biessy, Tony Bui, Lincoln MacKenzie, Jane E. Symonds, and Kirsty F. Smith. 2022. “Effects of Harmful Algal Blooms on Fish and Shellfish Species: A Case Study of New Zealand in a Changing Environment” Toxins 14, no. 5: 341. https://doi.org/10.3390/toxins14050341

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