Can cryptophyte abundance trigger toxic Karlodinium veneficum blooms in eutrophic estuaries?

Adolf, Jason E.; Bachvaroff, Tsvetan R.; Place, Allen R.

doi:10.1016/j.hal.2008.08.003

Cited by 106 publications

(96 citation statements)

References 73 publications

(99 reference statements)

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“…Although cryptophytes are considered a "high-quality" food, lacking hard exoskeleton structures or toxic metabolic products (Brett andMüller-Navarra 1997, Sterner andSchulz 1998), their higher content in bivalve food causes the red colouration of the tissue, making the mariculture products unfavourable for commercial needs (Pastoureaud et al 2003). Furthermore, cryptophytes are essential for the development of toxic or harmful blooms of some dinoflagellates (Adolf et al 2008) and ciliates (Peterson et al 2013). Such diverse interactions of cryptophytes with their environment and their importance for the marine food web emphasize the necessity for future monitoring of phytoplankton communities and environmental parameters in the area in order to detect the changes that might have a profound effect on the estuary's ecosystem dynamics and mariculture production.…”

Section: Discussionmentioning

confidence: 99%

Cryptophyte bloom in a Mediterranean estuary: High abundance of Plagioselmis cf. prolonga in the Krka River estuary (eastern Adriatic Sea)

et al. 2014

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Summary:During the June 2010 survey of phytoplankton and physicochemical parameters in the Krka River estuary (eastern Adriatic Sea), a cryptophyte bloom was observed. High abundance of cryptophytes (maximum 7.9×10 6 cells l -1 ) and high concentrations of the class-specific biomarker pigment alloxanthine (maximum 2312 ng l -1 ) were detected in the surface layer and at the halocline in the lower reach of the estuary. Taxonomical analysis revealed that the blooming species was Plagioselmis cf. prolonga. Analysis of the environmental parameters in the estuary suggested that the bloom was supported by the slower river flow as well as the increased orthophosphate and ammonium concentrations. The first record of a cryptophyte bloom in the Krka River estuary may indicate that large-scale changes are taking place in the phytoplankton community. Such changes could have a major impact on the natural ecosystem dynamics and the mariculture production in the area.Keywords: estuarine ecosystem; phytoplankton bloom; cryptophytes; chemotaxonomy; Mediterranean Sea; Krka River estuary.Proliferación de una criptófita en un estuario mediterráneo: alta abundancia de Plagioselmis cf. prolonga en el estuario del río Krka (Adriático) Resumen: Se observó una proliferación de una criptófita durante el estudio del fitoplancton y de los parámetros fisicoquími-cos en el estuario del río Krka (Adriático) en junio de 2010. La abundancia más alta de criptofitas (máximo 7.9×10 6 células l -1 ) y las mayores concentraciones del pigmento marcador específico de la clase, la aloxantina (máximo 2312 ng l -1 ), fueron detectados en la capa superficial y en la haloclina en el tramo inferior de la ría. El análisis taxonómico reveló que la especie que proliferó fue Plagioselmis cf. prolonga. El análisis de los parámetros ambientales del estuario sugirió que la proliferación estaba favorecida por el caudal lento del río, así como el aumento de las concentraciones de ortofosfato y amonio. El hecho de registrar por primera vez una proliferación de una criptófita en el estuario del río Krka podría indicar cambios a gran escala en la comunidad de fitoplancton. Tales cambios podrían tener un impacto importante en la dinámica de los ecosistemas naturales y la producción de la maricultura en la zona.Palabras clave: estuario; proliferación de fitoplancton; criptófitas; quimiotaxonomía; mar Mediterráneo; estuario del río Krka.Citation/Como citar este artículo: Šupraha L., Bosak S.,

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Section: Discussionmentioning

confidence: 99%

Cryptophyte bloom in a Mediterranean estuary: High abundance of Plagioselmis cf. prolonga in the Krka River estuary (eastern Adriatic Sea)

et al. 2014

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“…The species has been reported to produce a different substance with neurotoxic activity (Garcés et al, 2006), but the specific toxin has not been isolated and chemically characterised. While K. veneficum seems to prefer cryptophytes as food (Li et al, 1999;Adolf et al, 2008), K. armiger ingests most types of unicellular prey offered. It displays pronounced swarming behaviour and forms feeding aggregates when fed algal prey, allowing ingestion of prey several times larger than itself (Berge et al, 2008a).…”

Section: Introductionmentioning

confidence: 99%

“…Several aspects of its biology (Adolf et al, 2008), toxins (Deeds et al, 2002;Van Wagoner et al, 2010) and harmful effects on fish (Nielsen, 1993) have been described in detail and were recently reviewed (Place et al, 2011). The haemolytic and neurotoxic Karlotoxins (Deeds et al, 2002;Van Wagoner et al, 2010) produced by K. veneficum aid prey capture and are used directly to stun cryptophytes before ingestion (Sheng et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Marine microalgae attack and feed on metazoans

et al. 2012

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Free-living microalgae from the dinoflagellate genus Karlodinium are known to form massive blooms in eutrophic coastal waters worldwide and are often associated with fish kills. Natural bloom populations, recently shown to consist of the two mixotrophic and toxic species Karlodinium armiger and Karlodinium veneficum have caused fast paralysis and mortality of finfish and copepods in the laboratory, and have been associated with reduced metazooplankton biomass in-situ. Here we show that a strain of K. armiger (K-0688) immobilises the common marine copepod Acartia tonsa in a densitydependent manner and collectively ingests the grazer to promote its own growth rate. In contrast, four strains of K. veneficum did not attack or affect the motility and survival of the copepods. Copepod immobilisation by the K. armiger strain was fast (within 15 min) and caused by attacks of swarming cells, likely through the transfer and action of a highly potent but uncharacterised neurotoxin. The copepods grazed and reproduced on a diet of K. armiger at densities below 1000 cells ml, but above 3500 cells ml À 1 the mixotrophic dinoflagellates immobilised, fed on and killed the copepods. Switching the trophic role of the microalgae from prey to predator of copepods couples population growth to reduced grazing pressure, promoting the persistence of blooms at high densities. K. armiger also fed on three other metazoan organisms offered, suggesting that active predation by mixotrophic dinoflagellates may be directly involved in causing mortalities at several trophic levels in the marine food web.

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“…Roles of karlotoxins have been conjectured to mediate grazing pressures and as an allelochemical (13,14). However, on the basis of field data showing that cryptophyte's abundance precedes K. veneficum blooms (15) and laboratory feeding experiments demonstrating that only toxic strains are mixotrophic (16,17), hypothesized that karlotoxins provide advantages in prey capture. Here, we investigate whether and how karlotoxins are used during predation by measuring changes in swimming behavior of predators and prey.…”

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confidence: 99%

“…Four strains of K. veneficum (7,17) with identical genetic signatures (internal transcribed spacer sequence), two from Chesapeake Bay (MD5 and CCMP 1974) and two from estuaries south of Chesapeake Bay (BM1 and CCMP 2064), were examined. MD5 produces no detectable toxin and shows no mixotrophic behavior (15). Of the rest, 1974 produces KmTx-1 (0.3 pg/cell), whereas BM1 and 2064 produce KmTx-2 in a cell quota ranging from 1 to 2 pg/cell (5).…”

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confidence: 99%

A dinoflagellate exploits toxins to immobilize prey prior to ingestion

Sheng

Malkiel

Katz

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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Toxins produced by the harmful algal bloom (HAB) forming, mixotrophic dinoflagellate Karlodinium veneficum have long been associated with fish kills. To date, the perceived ecological role for toxins has been relief from grazing pressures. Here, we demonstrate that karlotoxins also serve as a predation instrument. Using high-speed holographic microscopy, we measure the swimming behavior of several toxic and nontoxic strains of K. veneficum and their prey, Storeatula major, within dense suspensions. The selected strains produce toxins with varying potency and dosages, including a nontoxic one. Results clearly show that mixing the prey with the predatory, toxic strains causes prey immobilization at rates that are consistent with the karlotoxins' potency and dosage. Even prey cells that continue swimming slow down after exposure to toxic predators. The swimming characteristics of predators vary substantially in pure suspensions, as quantified by their velocity, radii of helical trajectories, and direction of helical rotation. When mixed with prey, all toxic strains that are involved in predation slow down. Furthermore, they substantially reduced their predominantly vertical migration, presumably to remain in the vicinity of their prey. Conversely, the nontoxic control strain does not alter its swimming and does not affect prey behavior. In separate experiments, we show that exposing prey to exogenous toxins also causes prey immobilization at rates consistent with potency. Clearly, the toxic predatory strains use karlotoxins as a means of stunning their prey, before ingesting it. These findings add a substantiated critical understanding for why some HAB species produce such complex toxin molecules.digital holographic microscopy | karlotoxin | predator-prey interactions | harmful algal blooms

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Can cryptophyte abundance trigger toxic Karlodinium veneficum blooms in eutrophic estuaries?

Cited by 106 publications

References 73 publications

Cryptophyte bloom in a Mediterranean estuary: High abundance of <em>Plagioselmis</em> cf. <em>prolonga</em> in the Krka River estuary (eastern Adriatic Sea)

Cryptophyte bloom in a Mediterranean estuary: High abundance of <em>Plagioselmis</em> cf. <em>prolonga</em> in the Krka River estuary (eastern Adriatic Sea)

Marine microalgae attack and feed on metazoans

A dinoflagellate exploits toxins to immobilize prey prior to ingestion

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