Predator-induced defence in a dinoflagellate generates benefits without direct costs

Ryderheim, Fredrik; Selander, Erik; Kiørboe, Thomas

doi:10.1038/s41396-021-00908-y

Cited by 30 publications

(25 citation statements)

References 64 publications

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“…S3b). The presence of the (albeit variably) observed trade-off between growth and toxin production in response to copepod cues stands in contrast to a recent study which reported no cost to toxicity under varying levels of nitrogen limitation for the same strain of A. minutum (Ryderheim et al 2021). While these authors observed no reduction in growth rate, A. minutum cells shrank when exposed to copepodamides, an effect not seen in the current study.…”

Section: Discussioncontrasting

confidence: 99%

“…While these authors observed no reduction in growth rate, A. minutum cells shrank when exposed to copepodamides, an effect not seen in the current study. This discrepancy may be due to the higher cell densities and lower phosphate concentrations utilized (due to our use of K media) in the current study, compared to the study by Ryderheim and colleagues which used B1 media (Ryderheim et al 2021), which would be expected to intensify competition for a limiting resource (phosphate). The elevated competition in the current study explains the realized cost of toxin production in the form of reduced growth.…”

Section: Discussioncontrasting

confidence: 63%

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Predator cues target signaling pathways in toxic algal metabolome

Brown

Moore

Gaul

et al. 2022

Limnology & Oceanography

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Early detection of predators is critical to the survival of all living organisms. For phytoplankton, recognition and response to chemical cues from predators, as evidence of predation risk, are particularly crucial. The phytoplankton Alexandrium minutum upregulates its toxicity when exposed to copepodamides, a suite of compounds released by copepod predators. However, how A. minutum perceives these predatory cues and what metabolic pathways are involved in initiating toxin induction remains unknown. In this study, liquid chromatography‐mass spectrometry and NMR‐based metabolomics uncovered subtle physiological responses of A. minutum to copepodamides, including altered regulation of branched‐chain amino acid biosynthesis and potential enhancement of butanoate metabolism and arginine biosynthesis. While we have yet to identify a chemoreceptor directly activated by copepod cues, based on the results of inhibition experiments, detection of copepodamides appears to disrupt the activity of serine/threonine phosphatases leading to increased jasmonic acid biosynthesis and signaling, which leads to amplified gonyautoxin biosynthesis in A. minutum. This study is an important step toward a better understanding of chemosensory ecology of predator–prey interactions in phytoplankton.

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Section: Discussioncontrasting

confidence: 99%

Section: Discussioncontrasting

confidence: 63%

Predator cues target signaling pathways in toxic algal metabolome

Brown

Moore

Gaul

et al. 2022

Limnology & Oceanography

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“…Handling and selection of captured diatoms Feeding-current feeding copepods perceive particles that arrive in the feeding current individually as the particles come near the mechanoreceptory setae on the feeding appendages, which elicits a capture response (Koehl and Strickler 1981; Videos S1-S3). Copepods are known to be selective feeders, but prey selection appears to happen post capture while the prey is being handled by the feeding appendages, as demonstrated here for diatoms with different silica content, and elsewhere for dinoflagellates with different degrees of toxicity (Ryderheim et al 2021) or bioluminescence (Prevett et al 2019). The feeding appendages are equipped with both mechano-and chemosensors (Hallberg and Skog 2011) and both sensory modalities are probably involved in prey selection.…”

Section: Discussionmentioning

confidence: 65%

Thicker shells reduce copepod grazing on diatoms

Ryderheim

Grønning

Kiørboe

2022

Limnol Oceanogr Letters

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The diatom frustule provides partial protection against copepod grazing. Whether the defense is due to the cells being de‐selected or handled for so long that the grazers lose time for foraging is unknown. The mechanism has implications for the population dynamics of both defended and co‐occurring, undefended nutrient competitors. We use video‐observations to demonstrate that thick‐shelled diatoms captured by the copepod Temora longicornis were rejected more frequently than thin‐shelled diatoms, irrespective of cell size. The thick‐shelled cells of the larger diatoms were handled for much longer, and the time spent handling these limits the consumption of phytoplankton. This may be why many diatoms, even in the presence of dense grazer populations, reach bloom concentrations, and thus, facilitate aggregation and mass sedimentation. This has implications for both carbon sequestration and for securing a large population of cells at depth ready to colonize the pelagic, when growth conditions again become favorable.

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“…Theoretically there should be a cost associated with inducible defensive traits (Tollrian and Harvell, 1999), while defensive traits without costs are more likely to become constitutive (i.e., always present). However, some studies have been unable to establish costs of grazer induced traits in terms of reduced growth rate (Blossom et al, 2019;Ryderheim et al, 2021; but see Grønning and Kiørboe, 2020;Park and Dam, 2021). Our findings of reduced growth rate consequently suggests the presence of a direct allocation cost associated with expression of defensive traits, particularly in diatoms.…”

Section: Discussionmentioning

confidence: 58%

Species Specific Responses to Grazer Cues and Acidification in Phytoplankton- Winners and Losers in a Changing World

et al. 2022

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Phytoplankton induce defensive traits in response to chemical alarm signals from grazing zooplankton. However, these signals are potentially vulnerable to changes in pH and it is not yet known how predator recognition may be affected by ocean acidification. We exposed four species of diatoms and one toxic dinoflagellate to future pCO2 levels, projected by the turn of the century, in factorial combinations with predatory cues from copepods (copepodamides). We measured the change in growth, chain length, silica content, and toxin content. Effects of increased pCO2 were highly species specific. The induction of defensive traits was accompanied by a significant reduction in growth rate in three out of five species. The reduction averaged 39% and we interpret this as an allocation cost associated with defensive traits. Copepodamides induced significant chain length reduction in three of the four diatom species. Under elevated pCO2Skeletonema marinoi reduced silica content by 30% and in Alexandrium minutum the toxin content was reduced by 30%. Using copepodamides to induce defensive traits in the absence of direct grazing provides a straightforward methodology to assess costs of defense in microplankton. We conclude that copepodamide signalling system is likely robust to ocean acidification. Moreover, the variable responses of different taxa to ocean acidification suggest that there will be winners and losers in a high pCO2 world, and that ocean acidification may have structuring effects on phytoplankton communities.

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Predator-induced defence in a dinoflagellate generates benefits without direct costs

Cited by 30 publications

References 64 publications

Predator cues target signaling pathways in toxic algal metabolome

Predator cues target signaling pathways in toxic algal metabolome

Thicker shells reduce copepod grazing on diatoms

Species Specific Responses to Grazer Cues and Acidification in Phytoplankton- Winners and Losers in a Changing World

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