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


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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

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.


  1. 1

    Smetacek, V. Role of sinking in diatom life-history cycles: ecological, evolutionary and geological significance. Mar. Biol. 84, 239–251 (1985)

    Article  Google Scholar 

  2. 2

    Cushing, D. H. Marine Ecology and Fisheries (Cambridge Univ. Press, Cambridge, 1975)

    Google Scholar 

  3. 3

    Pohnert, G. Wound-activated chemical defence in unicellular planktonic algae. Angew. Chem. Int. Edn. 39, 4352–4354 (2000)

    CAS  Article  Google Scholar 

  4. 4

    Ianora, A., Poulet, S. A. & Miralto, A. The effects of diatoms on copepod reproduction: a review. Phycologia 42, 351–363 (2003)

    Article  Google Scholar 

  5. 5

    Verity, P. G. & Smetacek, V. Organism life cycles, predation, and structure of pelagic ecosystems. Mar. Ecol. Prog. Ser. 130, 277–293 (1996)

    ADS  Article  Google Scholar 

  6. 6

    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)

    ADS  Article  Google Scholar 

  7. 7

    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)

    Article  Google Scholar 

  8. 8

    Mauchline, J. The Biology of Calanoid Copepods (Academic, London, 1998)

    Google Scholar 

  9. 9

    Smetacek, V. The ocean's veil. Nature 419, 565 (2002)

    ADS  CAS  Article  Google Scholar 

  10. 10

    Ban, S. et al. The paradox of diatom copepod interactions. Mar. Ecol. Prog. Ser. 157, 287–293 (1997)

    ADS  Article  Google Scholar 

  11. 11

    Miralto, A. et al. The insidious effect of diatoms on copepod reproduction. Nature 402, 173–176 (1999)

    ADS  CAS  Article  Google Scholar 

  12. 12

    Irigoien, X. et al. Copepod hatching success in marine ecosystems with high diatom concentrations. Nature 419, 387–389 (2002)

    ADS  CAS  Article  Google Scholar 

  13. 13

    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)

    ADS  Article  Google Scholar 

  14. 14

    Poulet, S. A. et al. Reproductive response of Calanus helgolandicus. I. Abnormal embryonic and naupliar development. Mar. Ecol. Prog. Ser. 129, 85–95 (1995)

    ADS  Article  Google Scholar 

  15. 15

    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)

    CAS  Article  Google Scholar 

  16. 16

    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)

    CAS  Article  Google Scholar 

  17. 17

    Tosti, E. et al. Bioactive aldehydes from diatoms block the fertilization current in ascidian oocytes. Mol. Reprod. Dev. 66, 72–80 (2003)

    CAS  Article  Google Scholar 

  18. 18

    Romano, G. et al. A marine diatom-derived aldehyde induces apoptosis in copepod and sea urchin embryos. J. Exp. Biol. 206, 3487–3494 (2003)

    Article  Google Scholar 

  19. 19

    d'Ippolito, G. et al. New birth-control aldehydes from the diatom Skeletonema costatum: characterization and biogenesis. Tetrahedr. Lett. 43, 6133–6136 (2002)

    CAS  Article  Google Scholar 

  20. 20

    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)

    ADS  CAS  Article  Google Scholar 

  21. 21

    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)

    CAS  Article  Google Scholar 

  22. 22

    Tester, P. A. & Turner, J. T. Why is Acartia tonsa restricted to estuarine habitats? Bull. Plankton Soc. Jpn (Spec. Iss.) 603–611 (1991)

  23. 23

    Takai, M. et al. Structure–property relationship of α- and β-chitin. ACS Symp. Ser. 489, 38–52 (1992)

    CAS  Article  Google Scholar 

  24. 24

    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)

    ADS  Article  Google Scholar 

  25. 25

    Caldwell, G. S. Diatom Mediated Disruption of Invertebrate Reproduction and Development. PhD thesis, Univ. Newcastle-upon-Tyne (2004)

    Google Scholar 

  26. 26

    Kleppel, G. S. On the diets of calanoid copepods. Mar. Ecol. Prog. Ser. 99, 183–195 (1993)

    ADS  Article  Google Scholar 

  27. 27

    Wolfe, G. V. The chemical defense ecology of marine unicellular plankton: constraints, mechanisms, and impacts. Biol. Bull. 198, 225–244 (2000)

    CAS  Article  Google Scholar 

  28. 28

    Hamm, C. E. et al. Diatom cells are mechanically protected by their strong, lightweight, silica shells. Nature 421, 841–843 (2003)

    ADS  CAS  Article  Google Scholar 

  29. 29

    Yoshida, T. et al. Rapid evolution drives ecological dynamics in a predator–prey system. Nature 424, 303–306 (2003)

    ADS  CAS  Article  Google Scholar 

  30. 30

    Smetacek, V. A watery arms race. Nature 411, 745 (2002)

    ADS  Article  Google Scholar 

  31. 31

    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)

    CAS  Article  Google Scholar 

Download references


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.

Author information



Corresponding author

Correspondence to Adrianna Ianora.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

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)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

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).

Download citation

Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.