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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References
Smetacek, V. Role of sinking in diatom life-history cycles: ecological, evolutionary and geological significance. Mar. Biol. 84, 239–251 (1985)
Cushing, D. H. Marine Ecology and Fisheries (Cambridge Univ. Press, Cambridge, 1975)
Pohnert, G. Wound-activated chemical defence in unicellular planktonic algae. Angew. Chem. Int. Edn. 39, 4352–4354 (2000)
Ianora, A., Poulet, S. A. & Miralto, A. The effects of diatoms on copepod reproduction: a review. Phycologia 42, 351–363 (2003)
Verity, P. G. & Smetacek, V. Organism life cycles, predation, and structure of pelagic ecosystems. Mar. Ecol. Prog. Ser. 130, 277–293 (1996)
Miralto, A. et al. Inhibition of population growth in the copepods Acartia clausi and Calanus helgolandicus during diatom bloom. Mar. Ecol. Prog. Ser. 254, 253–268 (2003)
Colebrook, J. M. Continuous plankton records: seasonal variation in the distribution and abundance of plankton in the North Atlantic Ocean and the North Sea. J. Plankton Res. 4, 435–462 (1982)
Mauchline, J. The Biology of Calanoid Copepods (Academic, London, 1998)
Smetacek, V. The ocean's veil. Nature 419, 565 (2002)
Ban, S. et al. The paradox of diatom copepod interactions. Mar. Ecol. Prog. Ser. 157, 287–293 (1997)
Miralto, A. et al. The insidious effect of diatoms on copepod reproduction. Nature 402, 173–176 (1999)
Irigoien, X. et al. Copepod hatching success in marine ecosystems with high diatom concentrations. Nature 419, 387–389 (2002)
Weikert, H., Koppelmann, R. & Wiegratz, S. Evidence of episodic changes in deep-sea mesozooplankton abundance and composition in the Levantine Sea (Eastern Mediterranean). J. Mar. Syst. 30, 221–239 (2001)
Poulet, S. A. et al. Reproductive response of Calanus helgolandicus. I. Abnormal embryonic and naupliar development. Mar. Ecol. Prog. Ser. 129, 85–95 (1995)
Caldwell, G. S., Olive, P. J. W. & Bentley, M. G. Inhibition of embryonic development and fertilization in broadcast spawning marine invertebrates by water soluble diatom extracts and the diatom toxin 2-trans, 4-trans decadienal. Aquat. Toxicol. 60, 123–137 (2002)
Caldwell, G. S., Bentley, M. G. & Olive, P. J. W. The use of a brine shrimp (Artemia salina) bioassay to assess the toxicity of diatom extracts and short chain aldehydes. Toxicon 42, 301–306 (2003)
Tosti, E. et al. Bioactive aldehydes from diatoms block the fertilization current in ascidian oocytes. Mol. Reprod. Dev. 66, 72–80 (2003)
Romano, G. et al. A marine diatom-derived aldehyde induces apoptosis in copepod and sea urchin embryos. J. Exp. Biol. 206, 3487–3494 (2003)
d'Ippolito, G. et al. New birth-control aldehydes from the diatom Skeletonema costatum: characterization and biogenesis. Tetrahedr. Lett. 43, 6133–6136 (2002)
Pohnert, G. et al. Are volatile unsaturated aldehydes from diatoms the main line of chemical defence against copepods? Mar. Ecol. Prog. Ser. 245, 33–45 (2002)
Adolph, S., Poulet, S. A. & Pohnert, G. Synthesis and biological activity of α,β,γ,δ-unsaturated aldehydes from diatoms. Tetrahedron 59, 3003–3008 (2003)
Tester, P. A. & Turner, J. T. Why is Acartia tonsa restricted to estuarine habitats? Bull. Plankton Soc. Jpn (Spec. Iss.) 603–611 (1991)
Takai, M. et al. Structure–property relationship of α- and β-chitin. ACS Symp. Ser. 489, 38–52 (1992)
Turner, J. T. et al. Decoupling of copepod grazing rates, fecundity and egg-hatching success on mixed and alternating diatom and dinoflagellate diets. Mar. Ecol. Prog. Ser. 220, 187–199 (2001)
Caldwell, G. S. Diatom Mediated Disruption of Invertebrate Reproduction and Development. PhD thesis, Univ. Newcastle-upon-Tyne (2004)
Kleppel, G. S. On the diets of calanoid copepods. Mar. Ecol. Prog. Ser. 99, 183–195 (1993)
Wolfe, G. V. The chemical defense ecology of marine unicellular plankton: constraints, mechanisms, and impacts. Biol. Bull. 198, 225–244 (2000)
Hamm, C. E. et al. Diatom cells are mechanically protected by their strong, lightweight, silica shells. Nature 421, 841–843 (2003)
Yoshida, T. et al. Rapid evolution drives ecological dynamics in a predator–prey system. Nature 424, 303–306 (2003)
Smetacek, V. A watery arms race. Nature 411, 745 (2002)
Luo, X. P. et al. Determination of aldehydes and other lipid-peroxidation products in biological samples by gas-chromatography mass-spectrometry. Anal. Biochem. 228, 294–298 (1995)
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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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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DOI: https://doi.org/10.1038/nature02526
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