Copepod feeding response to varying Alexandrium spp. cellular toxicity and cell concentration among natural plankton samples

Teegarden, Gregory J.; Campbell, Robert G.; Anson, Dean T.; Ouellett, Aaron; Westman, Benjamin A.; Durbin, Edward G.

doi:10.1016/j.hal.2007.05.010

Cited by 40 publications

(39 citation statements)

References 23 publications

(41 reference statements)

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“…8-10). The inconclusive pattern of behavioral responses in our experiments aligns well with the results of the incubation experiments of (Teegarden et al, 2008): the very different feeding rates in 4 different species of copepods to Alexandrium spp. strains of different PST toxicity that they observed were unrelated to the level of total toxicity (as STX eq per cell) and only related to whether or not the cells were toxic.…”

Section: Potential Role Of Cellular Toxin Quantity and Composition Onsupporting

confidence: 87%

“…Some studies have demonstrated reduced growth and egg production rates (Colin and Dam, 2007;Dutz, 1998;Guisande et al, 2002;Roncalli et al, 2016;Sopanen et al, 2011;Teegarden et al, 2008) or elevated mortality (Avery et al, 2008;Sopanen et al, 2011) in copepods exposed to toxic algae compared to control algae. Such responses may be mediated by the behaviors considered above that both lead to reduced prey ingestion, or by the regurgitation of consumed algae, as described here for T. longicornis feeding on A. tamarense Alex2.…”

Section: Repertoire Of Copepod Feeding Behaviors and Implications To mentioning

confidence: 99%

“…Reported effects on copepods offered PST-containing Alexandrium spp., however, range from none to adverse effects on ingestion rate, egg production, egg hatching and offspring development duration (Dutz, 1998;Frangopulos et al, 2000;Guisande et al, 2002). These variations in responses are not related to the overall toxicity of the cells (Teegarden et al, 2008) and raises the question of whether or not the PSP toxins actually function as a grazer deterrents. Could other compounds produced by Alexandrium spp.…”

Section: Introductionmentioning

confidence: 99%

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Distinctly different behavioral responses of a copepod, Temora longicornis , to different strains of toxic dinoflagellates, Alexandrium spp.

Hansen

Nielsen

et al. 2017

Harmful Algae

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A B S T R A C TZooplankton responses to toxic algae are highly variable, even towards taxonomically closely related species or different strains of the same species. Here, the individual level feeding behavior of a copepod, Temora longicornis, was examined which offered 4 similarly sized strains of toxic dinoflagellate Alexandrium spp. and a non-toxic control strain of the dinoflagellate Protoceratium reticulatum. The strains varied in their cellular toxin concentration and composition and in lytic activity. High-speed video observations revealed four distinctly different strain-specific feeding responses of the copepod during 4 h incubations: (i) the 'normal' feeding behavior, in which the feeding appendages were beating almost constantly to produce a feeding current and most (90%) of the captured algae were ingested; (ii) the beating activity of the feeding appendages was reduced by ca. 80% during the initial 60 min of exposure, after which very few algae were captured and ingested; (iii) capture and ingestion rates remained high, but ingested cells were regurgitated; and (iv) the copepod continued beating its appendages and captured cells at a high rate, but after 60 min, most captured cells were rejected. The various prey aversion responses observed may have very different implications to the prey and their ability to form blooms: consumed but regurgitated cells are dead, captured but rejected cells survive and may give the prey a competitive advantage, while reduced feeding activity of the grazer may be equally beneficial to the prey and its competitors. These behaviors were not related to lytic activity or overall paralytic shellfish toxins (PSTs) content and composition and suggest that other cues are responsible for the responses.

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Section: Potential Role Of Cellular Toxin Quantity and Composition Onsupporting

confidence: 87%

Section: Repertoire Of Copepod Feeding Behaviors and Implications To mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Distinctly different behavioral responses of a copepod, Temora longicornis , to different strains of toxic dinoflagellates, Alexandrium spp.

Hansen

Nielsen

et al. 2017

Harmful Algae

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“…Copepods from historically exposed populations were less affected and able to acclimate to the exposure within a few days. Investigating the ingestion rate of Alexandrium cells added to natural plankton samples, Teegarden et al (2008) showed three of four tested copepod species to preferentially ingest non-toxic Alexandrium, but to avoid PSP toxin-producing species. Teegarden et al (2008) suggested that the magnitude of this response is dependent on both the cellular toxicity of Alexandrium and their abundance relative to non-toxic prey items.…”

Section: Aphanizomenon Flos-aqua)mentioning

confidence: 99%

“…Investigating the ingestion rate of Alexandrium cells added to natural plankton samples, Teegarden et al (2008) showed three of four tested copepod species to preferentially ingest non-toxic Alexandrium, but to avoid PSP toxin-producing species. Teegarden et al (2008) suggested that the magnitude of this response is dependent on both the cellular toxicity of Alexandrium and their abundance relative to non-toxic prey items. Further support for a grazer-deterring function of PSP toxins was provided by Selander et al (2006) who found that PSP toxin-producing dinoflagellates increase their cellular toxin content in response to waterborne cues from zooplankton grazers.…”

Section: Aphanizomenon Flos-aqua)mentioning

confidence: 99%

Grazer-induced toxin formation in dinoflagellates: a transcriptomic model study

Yang

Selander

Pavia

et al. 2011

European Journal of Phycology

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The cosmopolitan marine dinoflagellate Alexandrium minutum is known to produce toxins causing paralytic shellfish poisoning (PSP). As has recently been shown, this toxicity can be enhanced by the presence of certain copepod species. Inducible defences are known from a variety of marine organisms, but the associated transcriptomic changes have only been investigated in model angiosperms. Here, we use a microarray approach to investigate the changes in gene expression during the copepodprovoked induction of higher toxicity in A. minutum. We found a limited set of 14 genes (0.35% of the tested sequences) to be affected by copepod presence; gene expression changed by a factor of 1.9 to 11.4 when compared with control samples. We compared the differentially expressed genes after one day -before the onset of augmented toxicity -and after 3 days, when cellular toxin content in the induced samples was five times higher than in control cultures. Comparison with differences previously found between toxic and non-toxic strains revealed two sequences apparently associated with PSP toxin content. Our study is the first investigation of transcriptomic effects associated with grazer-induced induction of elevated toxicity in a protist. This provides a novel approach to the ecology of predator-prey interactions, as well as a highly targeted method for investigating the genes associated with toxin production and regulation in toxic dinoflagellates.

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Toxic dinoflagellates produce true grazer deterrents

Kiørboe

2018

Ecology

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Many phytoplankton species produce toxic substances, but their functional role is unclear. Specifically, it remains uncertain whether these compounds have a toxic or deterrent effect on grazers; only, the latter is consistent with toxins as defensive tools. Here, we show that 10 of 12 species or strains of toxic dinoflagellates were consumed at lower rates than a similarly sized nontoxic dinoflagellate by a copepod. Through video observations of individual prey-grazer interactions, we further demonstrate that the dominating mechanism is through capture, examination, and subsequent rejection of vital cells, that is, a true deterrent effect that offers a straightforward explanation to its evolution. We argue that the diversity of grazer responses to toxic phytoplankton reported in the literature, including toxic effects, and the high diversity of toxin profiles between strains of the same phytoplankton species reflect different stages of an ever-ongoing evolutionary arms race, facilitated by rapid adaptation of grazers to toxic substances. We further argue that defensive toxicity requires a chemical signal exterior to the cell that informs the grazer about the toxicity of the cell. The signal can be the toxin itself or just an aposematic signal of toxicity. In the former case, allelochemical effects may emerge at high cell concentrations as a nonadaptive side effect of a predator defenses.

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Copepod feeding response to varying Alexandrium spp. cellular toxicity and cell concentration among natural plankton samples

Cited by 40 publications

References 23 publications

Distinctly different behavioral responses of a copepod, Temora longicornis , to different strains of toxic dinoflagellates, Alexandrium spp.

Distinctly different behavioral responses of a copepod, Temora longicornis , to different strains of toxic dinoflagellates, Alexandrium spp.

Grazer-induced toxin formation in dinoflagellates: a transcriptomic model study

Toxic dinoflagellates produce true grazer deterrents

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