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Predator Chemical Cue Effects on the Diel Feeding Behaviour of Marine Protists

  • Environmental Microbiology
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Abstract

We have assessed the effect of copepod chemical cues on the diel feeding rhythms of heterotrophic and mixotrophic marine protists. All phagotrophic protists studied exhibited relatively high diurnal feeding rates. The magnitude of the diel feeding rhythm, expressed as the quotient of day and night ingestion rates, was inversely related to the time that phagotrophic protists were maintained in the laboratory in an environment without predators. In the case of the recently isolated ciliate Strombidium arenicola, the rhythm was lost after a few months. When challenged with chemical alarm signals (copepodamides) from the copepod Calanus finmarchicus at realistic concentrations (0.6–6 pM), S. arenicola partially re-established diurnal feeding. Conversely, the amplitude of the diel feeding rhythm for the ciliate Mesodinium rubrum was not affected by copepodamides, although the 24-h integrated food intake increased by approximately 23%. For the dinoflagellates Gyrodinium dominans and Karlodinium armiger, copepodamides significantly reduced the amplitude of their diel feeding rhythms; significant positive effects on total daily ingestion were only observed in G. dominans. Finally, the dinoflagellate Oxyrrhis marina, isolated >20 years ago, showed inconsistent responses to copepodamides, except for an average 6% increase in its total ingestion over 24 h. Our results demonstrate that the predation risk by copepods affects the diel feeding rhythm of marine protists and suggests a species-specific response to predation threats.

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Acknowledgements

We are grateful to all members of the research group Signals in the Sea for collaborating from the University of Gothenburg, with special thanks to Andrew Prevett for technical assistance and valuable help during laboratory work. We also want to thank Jan for the illustrations.

Graphics Program

All Figures have been elaborated using KaleidaGraph, except for Figure S2 which was elaborated with MATLAB.

Funding

This work was supported by the FERMI project (CGL2014-59227-R; MINECO/AEI/FEDER, UE) and is a contribution of the Marine Zooplankton Ecology Group (2017 SGR 87). AA was funded with an FPI fellowship (BES-2015-074092) from the MICINN of Spain.

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Authors and Affiliations

  1. Institut de Ciències del Mar (ICM-CSIC), Passeig Marítim de la Barceloneta 37-49, 08003, Barcelona, Spain

    Anna Arias, Enric Saiz & Albert Calbet

  2. Department of Marine Sciences, University of Gothenburg, Box 461, SE-450 30, Göteborg, Sweden

    Erik Selander

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  1. Anna Arias
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Contributions

AA and AC conceived and designed the experiments. AA performed the experiments. AA, AC, ESL, and ESZ participated in the data analysis. ESL contributed reagents and materials. AA, AC, and ESZ contributed to the statistical analyses. AA, AC, ESL, and ESZ wrote and gave final approval for the publication.

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Correspondence to Anna Arias.

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The authors declare that they have no conflict of interest.

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This article does not contain any studies with animals performed by any of the authors.

Supplementary Information

ESM 1

Supplementary information is available online at Microbial Ecology and includes (a) the functional response of the ciliate Strombidium arenicola, (b) a detailed explanation of the methodological process conducted to determine copepodamide effective concentrations and the resultant plot of copepodamide effective concentration throughout the incubation, and (3) a table containing day-time and night-time ingestion rates per grazer species studied in each experiment. Fig. S1 Ingestion rate of the ciliate Strombidium arenicola (μm3 grazer-1 h-1) as a function of prey concentration (μm3 mL-1). Error bars show standard error. Fig. S2 Effective concentration (nM) of copepodamides during 10h incubation. Closed circles represent the average data from the sampling time points and shaded area is the error interval (standard deviation). Table S1 Day and night ingestion rates (in terms of prey volume ingested, μm3 grazer-1 hour -1) for each of the studied grazer species as a function of copepodamides treatments (Control, 0.6 pM and 6 pM). Rates are differentiated between Experiment 1 and Experiment 2. Average ± standard error are shown. p-values from one-way ANOVA followed by a Dunnet’s test are presented to show the significance level of each copepodamides treatment with respect to the correspondent control in each phase (day and night). (DOCX 13264 kb)

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Arias, A., Selander, E., Saiz, E. et al. Predator Chemical Cue Effects on the Diel Feeding Behaviour of Marine Protists. Microb Ecol 82, 356–364 (2021). https://doi.org/10.1007/s00248-020-01665-9

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