Elsevier

Harmful Algae

Volume 103, March 2021, 102013
Harmful Algae

Original Article
Sublethal and antioxidant effects of six ichthyotoxic algae on early-life stages of the Japanese pearl oyster

https://doi.org/10.1016/j.hal.2021.102013Get rights and content

Highlights

  • The effects of exposure to six icthyotoxic algae on pearl oyster early-life stages were assessed.

  • Eggs, fertilization, embryos and larvae were differentially affected by the HAB.

  • H. circularisquama, H. akashiwo, Karenia spp., and M. polykrikoides affected eggs, fertilization and embryos.

  • Larval growth-specific effects of all HAB are reported, with increased GST activity but not SOD.

  • Cytotoxicty and detoxification could be associated with the effects.

Abstract

Several species of harmful algae form blooms that are detrimental to aquatic organisms worldwide with severe economic loss to several industries. The cosmopolitan ichthyotoxic dinoflagellates and raphidophytes Karenia spp., Chattonella spp., Heterosigma spp., and Margalefidinium (Cochlodinium) polykrikoides are known to cause mass mortalities of fish and invertebrates, and the dinoflagellates Heterocapsa spp. are known to cause mass mortalities of shellfish, notably bivalve molluscs. The species K. mikimotoi, K. papilionacea, H. circularisquama, H. akashiwo, M. polykrikoides, and C. marina form recurrent harmful algal blooms (HAB) in coastal aquaculture areas of shellfish, coinciding with the reproduction seasons of natural and farmed bivalve molluscs. In the present study, their effects on eggs, fertilization, embryos, and three larval stages (D-shaped, umbo and pre-settling larvae) of a model bivalve species, the Japanese pearl oyster, Pinctada fucata martensii, are reported. The harmful algae had differential negative effects on each developmental stage, and had differential effects on larvae depending on their growth stage. Eggs were more affected by M. polykrikoides, K. mikimotoi and H. circularisquama than H. akashiwo and K. papilionacea. Fertilized eggs and developing embryos were more affected by M. polykrikoides and H. circularisquama than K. mikimotoi, K. papilionacea and H. akashiwo. Mortalities as well as abnormalities were not observed in any larval stage; however, motility of d-larvae and umbo larvae was more reduced by H. circularisquama and C. marina, than M. polykrikoides. In elder, 16 day-old larvae, all harmful algae induced a significant decrease in motility with the most severe effect observed during exposures to H. circularisquama, C. marina, H. akashiwo and M. polykrikoides. The superoxidase dismutase activity in larvae was not affected by exposure to any harmful alga; however, 6- and 16-day old larvae experienced a significant increase in GST activity following 48 h of exposures, with higher sensitivity of the elder larvae to C. marina, K. mikimotoi and M. polykrikoides. These results indicate that all tested harmful algae are differentially detrimental to the early-life development of the Japanese pearl oyster, with involvement of oxidative stress. Both M. polykrikoides and H. circularisquama were the most toxic followed by C. marina, K. mikimotoi, H. akashiwo and K. papilionacea. In addition, more developed larvae were most sensitive to these harmful algae in terms of motility-avoidance behavior and oxidative stress response, suggesting that ingestion of the harmful algae might enhance the toxicity of contact-dependent effects and dissolved extracellular compounds. The results also showed that superoxide anions were not associated with effects observed in larvae. Instead cellular detoxification was induced. The differential, stage-specific and growth-specific sublethal effects on bivalve development and recruitment also warrant further investigations of the oxidative stress and antioxidant enzyme activities in larvae of bivalves, to better address the toxicity mechanisms of ichthyotoxic HAB and their impacts on the reproduction, recruitment, and fitness of bivalve molluscs.

Summary: The harmful algae Heterocapsa circularisquama, Chattonella marina, Hetrosigma akashiwo, Karenia mikimotoi, K. papilionacea, Margalefidinium (Cochlodinium) polykrikoides differentially affect early life stages of Japanese pearl oyster and activate detoxification enzymes in feeding larvae.

Section snippets

1. Introduction

Harmful algal blooms (HAB) have become widely distributed in aquatic environments, with clear trends of geographical expansions associated with anthropogenic activities, notably eutrophication, aquaculture activities, ship ballast waters, biofouling, climate change, and potentially microplastic pollution ((Hallegraeff and Bolch, 1991) Hallegraeff, 1993, 2010; Vitousek et al., 1997; Hamer et al., 2001; Anderson et al., 2002, 2012; Hégaret et al., 2008; (Glibert et al., 2014); Kudela et al., 2015

2.1. Biological material: algae and pearl oysters

The harmful algae Heterocapsa circularisquama, Chattonella marina, Heterosigma akashiwo, Karenia mikimotoi, K. papilionacea, and Margalefidinium polykrikoides were isolated from western Japan, and grown in autoclaved f/2 medium (Chen et al., 1969). All cultures were maintained under a 12 h light:12 h dark photoperiod, at 23 °C, and harvested at exponential growth phase for the exposure experiments. Algal cell densities were determined a priori. Sexually mature male and female pearl oysters,

3.1. Egg quality, fertilization success and embryo development

Quality of pearl oyster eggs was affected by exposure to Margalefidinium polykrikoides (Figs. 6 and 7), with abnormal membranes observed in 20.00 ± 2.85% of the exposed eggs. Except for exposure to C. marina, K. mikimotoi, M. polykrikoides, H. akashiwo and H. circularisquama induced spontaneous expulsion of polar bodies in 24.67 ± 1.45%, 20.00 ± 1.15%, 11.33 ± 1.45% and 8.97 ± 2.40%, respectively. Fertilization success, measured as the percentage of viable fertilized eggs that reached the

4. Discussion

In the present study, the effects of six ichthyototxic harmful algal bloom (HAB) species on eggs, fertilization, embryo development and three larval stages of the Japanese pearl oyster, Pinctada fucata martensii, were investigated, at realistically low cell densities and short durations of exposures. These species of HAB form recurrent blooms in coastal waters of Western Japan that last from a few days to a few months, at cell densities ranging from a few cells to several thousand cells per ml.

Author contributions

L. Basti conceived the experiments and acquired the funds; S. Nagai provided HAB cultures; L. Basti, J. Go, S. Okano, K. Higuchi, K. Nagai performed the experiments; L. Basti analyzed the enzymes and the data, and wrote the manuscript.

Declaration of Competing Interest

The authors declare no conflict of interest.

Acknowledgment

The research was supported by the Ministry of Education, Culture, Sports, Science and Technology (No. 17310027), and the Japan Society for the Promotion of Science through a Grant-In-Aid for Research Activity Start-up (15H06219).

References (109)

  • L.M. Grattan et al.

    Harmful algal blooms and public health

    Harmful Algae

    (2016)
  • G.M. Hallegraeff et al.

    Transport of toxic dinoflagellate cysts via ships’ ballast water

    Mar. Poll. Bull.

    (1991)
  • H. Hégaret et al.

    Combined effects of a parasite, QPX, and the harmful-alga, Prorocentrum minimum on northern quahogs, Mercenaria mercenaria

    Mar. Environ. Res.

    (2010)
  • H. Hégaret et al.

    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

    (2005)
  • H. Hégaret et al.

    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

    (2005)
  • D.S. Holland et al.

    Is a delay a disaster? Economic impacts of the delay of the California dunganess crab fishery due to harmful algal bloom

    Harmful Algae

    (2020)
  • D. Katsuo et al.

    A new and simple screening method for the detection of cytotoxic substances produced by harmful red tide phytoplankton

    Harmful Algae

    (2007)
  • D. Kim et al.

    Mechanism of superoxide anion generation in the toxic red tide phytoplankton Chattonella marina: possible involvement of NAD(P)H oxidase

    Biochim. Biophys. Acta Gen. Subj.

    (2000)
  • A. Kuroda et al.

    Isolation and characterization of light-dependent hemolytic cytotoxin from harmful red tide phytoplankton Chattonella marina

    Comp. Biochem. Physiol. C Toxicol. Pharmacol.

    (2005)
  • S. Martino et al.

    An approach to evaluating the economic impacts of harmful algal blooms: the effects of blooms Dinophysis spp. on the productivity of Scottish shellfish farms

    Harmful Algae

    (2020)
  • Y Matsuyama

    Impacts of the harmful dinoflagellate Heterocapsa circularisquama bloom on shellfish aquaculture in Japan and some experimental studies on invertebrates

    Harmful Algae

    (2012)
  • E. Nézan et al.

    Genetic diversity of the harmful family Kareniaceae (Gymnodiniales, Dinophyceae) in France, with the description of Karlodinium gentienii sp. nov.: A new potentially toxic dinoflagellate

    Harmful Algae

    (2014)
  • J. Ritzman et al.

    Economic and sociocultural impacts of fisheries closures in two fishing-dependent communities following the massive 2015 U.S. West Coast harmful algal bloom

    Harmful Algae

    (2018)
  • A. Rolton et al.

    Susceptibility of gametes and embryos of the eastern oyster, Crassostrea virginica, to Karenia brevis and its toxins

    Toxicon

    (2015)
  • A. Rolton et al.

    Effects of the red tide dinoflagellate, Karenia brevis, on early development of the eastern oyster Crassostrea virginica and northern quahog Mercenaria mercenaria

    Aquat. Toxicol.

    (2014)
  • M. Satake et al.

    Gymnocin-B with the largest contiguous polyether rings from the red tide dinoflagellate Karenia (formerly Gymnodinium) mikimotoi

    Tetrahedron Lett.

    (2005)
  • S.E. Shumway et al.

    The effects of the toxic dinoflagellate Protogonyaulax tamarensis on the feeding and behaviour of bivalve molluscs

    Aquat. Toxicol.

    (1987)
  • E. Siswanto et al.

    Detection of harmful algal blooms of Karenia mikimotoi using MODIS measurements: a case study of the Seto-Inland Sea

    Japan. Remote Sens. Environ.

    (2013)
  • R.B. Smith et al.

    Estimating the economic costs of algal blooms in the Canadian Lake Erie Basin

    Harmful Algae

    (2019)
  • Y.Z. Tang et al.

    Characterization of the toxicity of Cochlodinium polykrikoides isolates from Northeast US estuaries to finfish and shellfsih

    Harmful Algae

    (2009)
  • M.S. Ahmed et al.

    Properties of hemagglutinins newly separated from toxic phytoplankton

    Biochim. Biophys. Acta

    (1995)
  • R.G. Alscher et al.

    Role of superoxidases (SODs) in controlling oxidative stress in plants

    JBX

    (2002)
  • D.M. Anderson

    HABs in a changing world: a perspective on harmful algal blooms, their impacts, and research and management in a dynamic era of climactic and environmental change

  • D.M. Anderson et al.

    Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences

    Estuar. Coast.

    (2002)
  • K. Banno et al.

    Deleterious effects of harmful dinoflagellates and raphidophytes on egg viability and spermatozoa swimming velocity in the Japanese pearl oyster Pinctada fucata martensii

    J. Shellfish Res.

    (2018)
  • L. Basti et al.

    Physiological, pathological, and defense alterations in Manila clams (short-neck clams), Ruditapes philippinarum, induced by Heterocapsa circularisquama

    J. Shellfish Res.

    (2011)
  • L. Basti et al.

    Effects of the toxic dinoflagellate Heterocapsa circularisquama on larvae of the pearl oyster Pinctada fucata martensii (Dunker, 1873)

    J. Shellfish Res.

    (2011)
  • L. Basti et al.

    Harmful algal blooms and shellfish

  • L. Basti et al.

    Sensitivity of gametes, fertilization, and embryo development of the Japanese pearl oyster, Pinctada fucata martensii, to the harmful dinoflagellate, Heterocapsa circularisquama

    Mar. Biol.

    (2013)
  • L. Basti et al.

    Harmful algal blooms affect early-life stages of Japanese pearl oyster, Pinctada fucata martensii

  • L. Basti et al.

    Neuroenzymatic activity and physiological energetics in Manila clam, Ruditapes philippinarum, during short-term sublethal exposure to harmful alga, Heterocaspa circularisquama

    Aquat. Toxicol.

    (2016)
  • L. Basti et al.

    Mortalities of the short-neck clam Ruditapes philippinarum induced by the toxic dinoflagellate Heterocapsa circularisquama

    Fish. Sci.

    (2010)
  • L.H. Booth et al.

    A comparison of biomarker responses in the earthworm Aporrectodea caliginosa to the organophosphorous insecticides diazinon and chlorpyrifos

    Environ. Toxicol. Chem.

    (2001)
  • V.M. Bricelj et al.

    Comparative physiological and behavioral responses to PSP toxins in two bivalve molluscs, the softshell clam, Mya arenaria, and surfclam, Spisula solidissima

  • L.C.M. Chen et al.

    Bonnemaisonia hamifera Hariot in nature and in culture

    J. Phycol.

    (1969)
  • K. Cho et al.

    Haemolytic activity and reactive oxygen species production of four harmful algal bloom species

    European J. Phycol.

    (2017)
  • K. Dauson et al.

    Regional economic impacts of razor clam beach closures due to harmful algal blooms (HABs) on the Pacific coast of Washington. 2010

    Harmful Algae

    (2010)
  • J.J. Dorantes-Aranda et al.

    Progress in understanding algal bloom-mediated fish kills: the role of superoxide radicals, phycotoxins and fatty acids

    PLoS ONE

    (2015)
  • B. Edvardsen et al.

    The Ecology of Harmful Flagellates within Prymnesiophyceae and Raphidophyceae

  • E. Erard-LeDenn et al.

    Effects of Gyrodinium cf. aureolum on Pecten maximus (post larvae, juveniles and adults).

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