Intoxicated copepods: ingesting toxic phytoplankton leads to risky behaviour

Lasley-Rasher, Rachel; Nagel, Kathryn; Angra, Aakanksha; Yen, Jeannette

doi:10.1098/rspb.2016.0176

Cited by 18 publications

(17 citation statements)

References 62 publications

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“…The brine shrimps exposed to the toxic dinoflagellates exhibited reduced swimming activity, ultimately immobility. Swimming behavior has a direct impact on zooplankton dispersal, encounter with prey and predators, and vulnerability to predation which determine the propensity of individuals to graze on harmful species and transfer phycotoxins through the food web [36]. Only ~20% of A .…”

Section: Discussionmentioning

confidence: 99%

“…Differential survival rates of toxin-exposed individuals may indicate some degree of toxin resistance by individuals selected in natural populations in the long-term [36, 37]. From an ecological point of view, toxin-resistant zooplankton fed harmful alga are more hazardous than sensitive individuals by its higher capacity for toxin accumulation which favors toxin transfer to higher consumers and dispersion of toxins through marine environments.…”

Section: Introductionmentioning

confidence: 99%

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Toxicity of benthic dinoflagellates on grazing, behavior and survival of the brine shrimp Artemia salina

et al. 2017

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Harmful algae may differently affect their primary grazers, causing sub-lethal effects and/or leading to their death. The present study aim to compare the effects of three toxic benthic dinoflagellates on clearance and grazing rates, behavioral changes, and survival of Artemia salina. Feeding assays consisted in 1-h incubations of brine shrimps with the toxic Prorocentrum lima, Gambierdiscus excentricus and Ostreopsis cf. ovata and the non-toxic Tetraselmis sp. Brine shrimps fed unselectively on all toxic and non-toxic algal preys, without significant differences in clearance and ingestion rates. Acute toxicity assays were performed with dinoflagellate cells in two growth phases during 7-h to assess differences in cell toxicity to A. salina. Additionally, exposure to cell-free medium was performed to evaluate its effects on A. salina survival. The behavior of brine shrimps significantly changed during exposure to the toxic dinoflagellates, becoming immobile at the bottom by the end of the trials. Dinoflagellates significantly affected A. salina survival with 100% mortality after 7-h exposure to cells in exponential phase (all treatments) and to P. lima in stationary phase. Mortality rates of brine shrimps exposed to O. cf. ovata and G. excentricus in stationary phase were 91% and 75%, respectively. However, incubations of the brine shrimps with cell-free medium did not affect A. salina survivorship. Significant differences in toxic effects between cell growth phases were only found in the survival rates of A. salina exposed to G. excentricus. Acute exposure to benthic toxic dinoflagellates induced harmful effects on behavior and survival of A. salina. Negative effects related to the toxicity of benthic dinoflagellates are thus expected on their primary grazers making them more vulnerable to predation and vectors of toxins through the marine food webs.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Toxicity of benthic dinoflagellates on grazing, behavior and survival of the brine shrimp Artemia salina

et al. 2017

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“…For mechanosensitive predators, flow perturbations generated by hydrodynamically conspicuous swimming behaviors seen here could lead to preferential predation of copepod grazers; in some cases this could also establish a trophic vector by which toxins accumulate in upper trophic levels (Teegarden et al ), although it should be noted that K. brevis is directly icthyotoxic (Landsberg ). Gannon et al () speculate that reduced fish abundance in a Florida HAB ( K. brevis ) may have been at least partially due to increased predation on zooplankton caused by neurotoxic influences that produce erratic swimming (e.g., Lasley‐Rasher et al ). Our results suggest that such behaviors may occur when zooplankton detect and respond to HAB‐containing thin layers in addition to effects on swimming caused by ingesting harmful algal species.…”

Section: Discussionmentioning

confidence: 99%

Copepod avoidance of thin chemical layers of harmful algal compounds

True

Webster

Weissburg

et al. 2017

Limnology & Oceanography

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In a physical model of a thin planktonic layer, the estuarine copepod Acartia tonsa strongly avoided weakly stratified layers of dissolved chemical compounds from the harmful dinoflagellate Karenia brevis. Chemical‐induced changes in swimming kinematics allowed copepods to effectively avoid the layer and surrounding volume, highlighting the relevance of harmful alga‐grazer interactions at a distance that involve dissolved chemical signals. Avoidance increased significantly with increasing chemical concentration representative of a range of ecologically relevant bloom conditions (1–104 cells/mL equivalent). Under mid to maximal bloom conditions, Acartia displayed visually and hydrodynamically conspicuous avoidance jumps featuring large, rapid displacements with swimming speeds near those reported for predatory escape reactions. Previous findings show K. brevis is both toxic and nutritionally inadequate to A. tonsa when ingested and that exposure to dissolved chemical compounds likely rapidly suppresses effective sampling and grazing behaviors. Thus, copepods have strong incentive to sense and avoid nearby, spatially discrete patches of toxic algae in order to improve fitness by avoiding exposure and/or ingestion and associated negative impacts. Our results suggest harmful alga not only produce deleterious physiological effects in copepod grazers, but chemical‐induced behavioral responses also likely alter grazer distributions and top‐down control via avoidance reactions (reduced harmful alga‐grazer encounter rates). Additionally, predator‐prey encounter rates at higher trophic levels are likely enhanced via significant changes in copepod swimming kinematics. These combined mechanisms could protect and sustain harmful blooms contained in subsurface thin layers until blooms reach critical mass and produce widespread impacts at the ecosystem level, the “cryptic bloom” effect.

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“…), while many reports demonstrate toxic effects (Sykes and Huntley , Lasley‐Rasher et al. , Rasmussen et al. , Xu et al.…”

Section: Introductionmentioning

confidence: 99%

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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Intoxicated copepods: ingesting toxic phytoplankton leads to risky behaviour

Cited by 18 publications

References 62 publications

Toxicity of benthic dinoflagellates on grazing, behavior and survival of the brine shrimp Artemia salina

Toxicity of benthic dinoflagellates on grazing, behavior and survival of the brine shrimp Artemia salina

Copepod avoidance of thin chemical layers of harmful algal compounds

Toxic dinoflagellates produce true grazer deterrents

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