Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom

Abstract

The growth cycle in nutrient-rich, aquatic environments starts with a diatom bloom that ends in mass sinking of ungrazed cells and phytodetritus1. The low grazing pressure on these blooms has been attributed to the inability of overwintering copepod populations to track them temporally2. We tested an alternative explanation: that dominant diatom species impair the reproductive success of their grazers. We compared larval development of a common overwintering copepod fed on a ubiquitous, early-blooming diatom species with its development when fed on a typical post-bloom dinoflagellate. Development was arrested in all larvae in which both mothers and their larvae were fed the diatom diet. Mortality remained high even if larvae were switched to the dinoflagellate diet. Aldehydes, cleaved from a fatty acid precursor by enzymes activated within seconds after crushing of the cell3, elicit the teratogenic effect4. This insidious mechanism, which does not deter the herbivore from feeding but impairs its recruitment, will restrain the cohort size of the next generation of early-rising overwinterers. Such a transgenerational plant–herbivore interaction could explain the recurringly inefficient use of a predictable, potentially valuable food resource—the spring diatom bloom—by marine zooplankton.

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Figure 1: Effects of combinations of maternal and neonate diets on development rates (a, c, e) and percentage survivorship (b, d, f) of C. helgolandicus larvae.
Figure 2: Percentage survivorship of C. helgolandicus nauplii spawned from wild females during the winter/spring bloom of 2003 in the North Adriatic Sea, and successively reared on the diatom S. costatum (SKE) or the dinoflagellate P. minimum (PRO).
Figure 3: Effects of diet on C. helgolandicus offspring fitness.
Figure 4: The effects of the aldehyde DD on development and percentage survivorship of C. helgolandicus.

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Acknowledgements

We thank F. Esposito for the preparation of algal cultures and assistance in feeding and rearing experiments. Thanks are also due to F. Palumbo, M. Perna, M. Di Pinto, J. M. Roualec and P. Quemener for technical assistance at sea. The authors acknowledge the financial contribution of their respective Institutes, and G.P. and T.W. also acknowledge that of the Deutsche Forschungsgemeinschaft. This paper represents a contribution towards the aims of MARBEF. MARBEF is an EU Network of excellence on Marine Biodiversity and Ecosystem Functioning under EU-Framework Programme 6.

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Correspondence to Adrianna Ianora.

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Supplementary information

Supplementary Information 1

Supplementary Table 1 shows t-Test results of duration time for each developmental stage of Calanus helgolandicus. Supplementary Table 2 shows t-Test results of the mean number of surviving C. helgolandicus juveniles. (DOC 39 kb)

Supplementary Information 2

Supplementary Figure 1 and Methods concerning the amount of decadienal (DD) uptake by Calanus helgolandicus feeding on DD-treated Prorocentrum minimum (PRO). (DOC 273 kb)

Supplementary Information 3

Supplementary Figure 2 and Methods concerning complementary tests of the effects of decadienal (DD) on undifferentiated and differentiated mammalian (A1 mes c-myc) cell lines (DOC 440 kb)

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Ianora, A., Miralto, A., Poulet, S. et al. Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom. Nature 429, 403–407 (2004). https://doi.org/10.1038/nature02526

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