Marine Biology

, Volume 158, Issue 9, pp 1965–1980 | Cite as

Strain-related physiological and behavioral effects of Skeletonema marinoi on three common planktonic copepods

  • Roswati Md Amin
  • Marja Koski
  • Ulf Båmstedt
  • Charles Vidoudez
Original Paper


Three strains of the chain-forming diatom Skeletonema marinoi, differing in their production of polyunsaturated aldehydes (PUA) and nutritional food components, were used in experiments on feeding, egg production, hatching success, pellet production, and behavior of three common planktonic copepods: Acartia tonsa, Pseudocalanus elongatus, and Temora longicornis. The three different diatom strains (9B, 1G, and 7J) induced widely different effects on Acartia tonsa physiology, and the 9B strain induced different effects for the three copepods. In contrast, different strains induced no or small alterations in the distribution, swimming behavior, and turning frequency of the copepods. 22:6(n-3) fatty acid (DHA) and sterol content of the diet typically showed a positive effect on either egg production (A. tonsa) or hatching success (P. elongatus), while other measured compounds (PUA, other long-chain polyunsaturated fatty acids) of the algae had no obvious effects. Our results demonstrate that differences between strains of a given diatom species can generate effects on copepod physiology, which are as large as those induced by different algae species or groups. This emphasizes the need to identify the specific characteristics of local diatoms together with the interacting effects of different mineral, biochemical, and toxic compounds and their potential implications on different copepod species.


Swimming Speed Hatching Success Skeletonema Food Patch Copepod Species 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors wish to thank the Nordic Marine Academy, the Ministry of Higher Education, Malaysia and University Malaysia Terengganu for funding. We also thank Johanna Bergkvist for providing the Skeletonema marinoi strains; Thomas Kiørboe and Hans Henrik Jacobsen for methodological guidance; Erik Lundberg and Tommy Olofsson for chemical analysis. The use of laboratory facilities at Denmark Technical University is gratefully acknowledged.

Open Access

This article is distributed under the terms of the Creative Commons Attribution Noncommercial License which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.


  1. Ask J, Reinkainen M, Båmstedt U (2006) Variation in hatching success and egg production of Eurytemora affinis (Calanoida, Copepoda) from the Gulf of Bothnia, Baltic Sea, in relation to abundance and clonal differences of diatoms. J Plankton Res 28:683–694CrossRefGoogle Scholar
  2. Ban S, Burns C, Castel J, Chaudron Y, Christou E, Escribano R, Umani S, Gasparini S, Guerro-Ruiz F, Hoffmeyer M, Ianora A, Kang H-K, Laabir M, Lacoste A, Miralto A, Ning X, Poulet S, Rodriguez V, Runge J, Shi J, Starr M, Uye S, Wang Y (1997) The paradox of diatom-copepod interactions. Mar Ecol Prog Ser 157:287–293CrossRefGoogle Scholar
  3. Barofsky A, Vidoudez C, Pohnert G (2009) Metabolic profiling reveals growth stage variability in diatom exudates. Limnol Oceanogr Methods 7:382–390CrossRefGoogle Scholar
  4. Bochdasky AB, Bollen SM (2004) Relevant scales in zooplankton ecology: distribution, feeding, and reproduction of the copepod Acartia hudsonica in response to thin layers of the diatom Skeletonema costatum. Limnol Oceanogr 49:625–635CrossRefGoogle Scholar
  5. Broglio E, Jónasdóttir SH, Calbet A, Jakobsen HH, Saiz E (2003) Effect of heterotrophic versus autotrophic food on feeding and reproduction of the calanoid copepod Acartia tonsa: relationship with prey fatty acid composition. Mar Ecol Prog Ser 31:267–278Google Scholar
  6. Buskey EJ (1984) Swimming pattern as an indicator of the roles of copepod sensory systems in the recognition of food. Mar Biol 79:165–175CrossRefGoogle Scholar
  7. Cohen JH, Tester PA, Richard B, Forward RB Jr (2007) Sublethal effects of the toxic dinoflagellate Karenia brevis on marine copepod behavior. J Plankton Res 29:301–315CrossRefGoogle Scholar
  8. Crockett EL, Hassett RP (2005) A cholesterol-enriched diet enhances egg production and egg viability without altering cholesterol content of biological membranes in the copepod Acartia hudsonica. Physiol Biochem Zool 78:424–433CrossRefGoogle Scholar
  9. Dagg M (1977) Some effects of patchy food environments on copepods. Limnol Oceanogr 22:99–107CrossRefGoogle Scholar
  10. Daro MH (1988) Migratory and grazing behavior of copepods and vertical distribution of phytoplankton. Bull Mar Sci 43:710–729Google Scholar
  11. Dutz J, Koski M, Jónasdóttir SH (2008) Copepod reproduction is unaffected by diatom aldehydes or lipid composition. Limnol Oceanogr 53:225–235CrossRefGoogle Scholar
  12. Ederington MC, Mcmanus GB, Harvey HR (1995) Trophic transfer of fatty acids, sterols, and a triterpenoid alcohol between bacteria, a ciliate, and the copepod Acartia tonsa. Limnol Oceanogr 40:860–867CrossRefGoogle Scholar
  13. Evjemo JO, Tokle N, Vadstein O, Olsen Y (2008) Effect of essential dietary fatty acids on egg production and hatching success of the marine copepod Temora longicornis. J Exp Mar Biol Ecol 365:31–37CrossRefGoogle Scholar
  14. Fontana A, d’Ippolito G, Cutignano A, Romano G, Ianora A, Miralto A, Cimino G (2007a) Oxylipin pathways in marine diatoms: a look at the chemical aspects. Pure Appl Chem 79:481–490CrossRefGoogle Scholar
  15. Fontana A, d’Ippolito G, Cutignano A, Romano G, Lamari N, Massa Gallucci A, Cimino G, Miralto A, Ianora A (2007b) LOX-induced lipid peroxidation as mechanism responsible for the detrimental effect of marine diatoms on zooplankton grazers. Chem BioChem 8:1810–1818Google Scholar
  16. Frost BW (1972) Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnol Oceanogr 17:805–815CrossRefGoogle Scholar
  17. Hasset RP (2004) Supplementation of a diatom diet with cholesterol can enhance copepod egg production rates. Limnol Oceanogr 49:488–494CrossRefGoogle Scholar
  18. Holste L, St. John MA, Peck MA (2009) The effects of temperature and salinity on reproductive success of Temora longicornis in the Baltic Sea: a copepod coping with a tough situation. Mar Biol 156:527–540CrossRefGoogle Scholar
  19. Ianora A, Poulet SA, Miralto A (2003) The effects of diatoms on copepod reproduction: a review. Phycologia 42:351–363CrossRefGoogle Scholar
  20. Ianora A, Miralto A, Poulet SA, Carotenuto Y, Buttino I, Romano G, Casotti R, Pohnert G, Wichard T, Colucci-D’Amato L, Terrazzano G, Smetacek V (2004) Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom. Nature 429:403–407CrossRefGoogle Scholar
  21. Ianora A, Caotti R, Bastianini M, Brunet C, d’Ippolito G, Acri F, Fontana A, Cutignano A, Turner J, Miralto A (2009) Low reproductive success for copepods during a bloom of the non-aldehyde-producing diatom Cerataulina pelagica in the North Adriatic Sea. Mar Ecol 29:399–411CrossRefGoogle Scholar
  22. Ianora A, Romano G, Carotenuto Y, Esposito F, Roncalli V, Buttino I, Miralto A (2010) Impact of the diatom oxylipin 15S-HEPE on the reproductive success of the copepod Temora stylifera. Hydrobiologia. doi:  10.1007/s10750-010-0420-7 CrossRefGoogle Scholar
  23. Irigoien X, Harris RP, Verheye HM, Joly P, Runge J, Starr M, Pond D, Campbell R, Shreeve R, Ward P, Smith AN, Dam HG, Peterson W, Tirelli V, Koski M, Smith T, Harbour D, Davidson R (2002) Copepod hatching success in marine ecosystems with high diatom concentrations. Nature 419:387–389CrossRefGoogle Scholar
  24. Irigoien X, Huisman J, Harris RP (2004) Global biodiversity patterns of marine phytoplankton and zooplankton. Nature 429:864–867CrossRefGoogle Scholar
  25. Jónasdóttir SH (1994) Effects of food quality on the reproductive success of Acartia tonsa and Acartia hudsonica: laboratory observations. Mar Biol 121:67–81CrossRefGoogle Scholar
  26. Jónasdóttir SH, Kiørboe T (1996) Copepod recruitment and food composition: do diatoms affect hatching success? Mar Biol 125:743–750CrossRefGoogle Scholar
  27. Jónasdóttir S, Visser AW, Jespersen C (2009) Assessing the role of food quality in the production and hatching of Temora longicornis eggs. Mar Ecol Prog Ser 382:139–150CrossRefGoogle Scholar
  28. Jónasdóttir S, Dutz J, Koski M, Yebra L, Jakobsen HH, Vidoudez C, Pohnert G, Nejstgaard JC (2011) Extensive cross disciplinary analysis of biological and chemical control of Calanus finmarchicus reproduction during an aldehyde forming diatom bloom in mesocosms. Mar Biol. doi: 10.1007/s00227-011-1705-8 CrossRefGoogle Scholar
  29. Jones RH, Flynn KJ (2005) Nutritional status and diet composition affects the nutritional value of diatoms as copepod prey. Science 307:1457–1458CrossRefGoogle Scholar
  30. Kiørboe T (1989) Phytoplankton growth rate and nitrogen content: implications for feeding and fecundity in a herbivorous copepod. Mar Ecol Prog Ser 55:229–234CrossRefGoogle Scholar
  31. Kiørboe T (2007) Mate finding, mating, and population dynamics in a planktonic copepod Oithona davisae: there are too few males. Limnol Oceanogr 52:1511–1522CrossRefGoogle Scholar
  32. Kiørboe T, Møhlenberg F, Riisgård HU (1985) In situ feeding rates of planktonic copepods: a comparison of four methods. J Exp Mar Biol Ecol 88:67–81CrossRefGoogle Scholar
  33. Klein Breteler WCM, Fransz HG, Gonzalez SR (1982) Growth and development of four calanoid copepod species under experimental and natural conditions. Neth J Sea Res 16:195–207CrossRefGoogle Scholar
  34. Klein Breteler WCM, Schogt N, Baas M, Schouten S, Kraay GW (1999) Trophic upgrading of food quality by protozoans enhancing copepod growth: role of essential lipids. Mar Biol 135:191–198CrossRefGoogle Scholar
  35. Klein Breteler WCM, Schogt N, Rampen S (2005) Effect of diatom nutrient limitation on copepod development: role of essential lipids. Mar Ecol Prog Ser 291:25–133CrossRefGoogle Scholar
  36. Kleppel GS, Burkart CA (1995) Egg production and nutritional environment of Acartia tonsa: the role of food quality in copepod nutrition. ICES J Mar Sci 52:297–304CrossRefGoogle Scholar
  37. Kleppel GS, Burkart CA, Houchin L (1998) Nutrition and the regulation of egg production in the calanoid copepod Acartia tonsa. Limnol Oceanogr 43:1000–1007CrossRefGoogle Scholar
  38. Koski M, Breteler WK (2003) Influence of diet on copepod survival in the laboratory. Mar Ecol Prog Ser 264:73–82CrossRefGoogle Scholar
  39. Koski M, Breteler WK, Schogt N, Gonzalez S, Jakobsen HH (2006) Life-stage-specific differences in exploitation of food mixtures: diet mixing enhances copepod egg production but not juvenile development. J Plankton Res 28:919–936CrossRefGoogle Scholar
  40. Koski M, Richard T, Jónasdóttir S (2008) ‘‘Good’’ and ‘‘bad’’ diatoms: development, growth and juvenile mortality of the copepod Temora longicornis on diatom diets. Mar Biol 154:719–734CrossRefGoogle Scholar
  41. Lee RF, Hagen W, Kattner G (2006) Lipid storage in marine zooplankton. Mar Ecol Prog Ser 307:273–306CrossRefGoogle Scholar
  42. Leising AW (2002) Copepod foraging in thin layers using SEARCH (Simulator for Exploring Area-Restricted search in Complex Habitats). Mar Model 2:1–18CrossRefGoogle Scholar
  43. Leising AW, Franks PJS (2000) Copepod vertical distribution within a spatially variable food source: a simple foraging strategy model. J Plankton Res 22:999–1024CrossRefGoogle Scholar
  44. Lester K, Heil C, Neely M, Spence D, Murasko S, Hopkins T, Sutton T, Burghart S, Bohrer R, Remsen A (2008) Zooplankton and Karenia brevis in the Gulf of Mexico. Cont Shelf Res 28:99–111CrossRefGoogle Scholar
  45. Mayzaud P, Roche-Mayzaud O, Razouls S (1992) Medium term time acclimation of feeding and digestive enzyme activity in marine copepods: influence of food concentration and copepod species. Mar Ecol Prog Ser 89:197–212CrossRefGoogle Scholar
  46. Miralto A, Barone G, Romano G, Poulet SA, Ianora A, Russo L, Buttino I, Mazzarella G, Laabir M, Cabrini M, Giacobbe MG (1999) The insidious effect of diatoms on copepod reproduction. Nature 402:173–176CrossRefGoogle Scholar
  47. Peters J, Dutz J, Hagen W (2007) Role of essential fatty acids on the reproductive success of the copepod Temora longicornis in the North Sea. Mar Ecol Prog Ser 341:153–163CrossRefGoogle Scholar
  48. Pierson JJ, Halsband-Lenk C, Leising AW (2005) Reproductive success of Calanus pacificus during diatom blooms in Dabob Bay, Washington. Prog Oceanogr 67:314–331CrossRefGoogle Scholar
  49. Pohnert G, Lumineau O, Cueff A, Adolph S, Cordevant C, Lange M (2002) Are volatile unsaturated aldehydes from diatoms the main line of chemical defence against copepods. Mar Ecol Prog Ser 245:33–45CrossRefGoogle Scholar
  50. Poulet SA, Wichard T, Ledoux JB, Lebreton B, Marchetti J, Dancie C, Bonnet D, Cueff A, Morin P, Pohnert G (2006) Influence of diatoms on copepod reproduction. I. Field and laboratory observations related to Calanus helgolandicus egg production. Mar Ecol Prog Ser 308:129–142CrossRefGoogle Scholar
  51. Renz J, Hirche HJ (2006) Life cycle of Pseudocalanus acuspes Giesbrecht (Copepoda, Calanoida) in the Central Baltic Sea: I. seasonal and spatial distribution. Mar Bio 148:567–580CrossRefGoogle Scholar
  52. Runge JA, Roff JC (2000) The measurement of growth and reproductive rates. In: Harris R (ed) ICES zooplankton methodology manual. Academic, New York, pp 401–454CrossRefGoogle Scholar
  53. Rynearson TA, Newton JA, Armbrust EV (2006) Spring bloom development, genetic variation, and population succession in the planktonic diatom Ditylum brightwelli. Limnol Oceanogr 51:1249–1261CrossRefGoogle Scholar
  54. Saravanan V, Godhe A (2010) Genetic heterogeneity and physiological variation among seasonally separated clones of Skeletonema marinoi (Bacillariophyceae) in the Gullmar Fjord, Sweden. Eur J Phycol 45:177–190CrossRefGoogle Scholar
  55. Sarno D, Kooistra HCF, Medlin LK, Percopo I, Zingone A (2005) Diversity of the genus Skeletonema (Bacillariophyceae). II. An assessment of the taxonomy of S. costatum-like species with the descrpution of four new species. J Phycol 41:151–176CrossRefGoogle Scholar
  56. Shin K, Jang MC, Jang PK, Ju SJ, Lee TK, Chang M (2003) Influence of food quality on egg production and viability of the marine planktonic copepod Acartia omorii. Prog Oceanogr 57:265–277CrossRefGoogle Scholar
  57. Steele JH (1974) The structure of marine ecosystems. Harvard University Press, CambridgeCrossRefGoogle Scholar
  58. Støttrup JG, Jensen J (1990) Influence of algal diet on feeding and egg-production of the calanoid copepod Acartia tonsa Dana. J Exp Mar Biol Ecol 141:87–105CrossRefGoogle Scholar
  59. Taylor RL, Abrahamsson K, Godhe A, Wängberg S-Å (2009) Seasonal variability in polyunsaturated aldehyde production potential between strains of Skeletonema marinoi (Bacillariophyceae). J Phycol 45:46–53CrossRefGoogle Scholar
  60. Tiselius P (1992) Behavior of Acartia tonsa in patchy food environments. Limnol Oceanogr 37:1640–1651CrossRefGoogle Scholar
  61. Tiselius P, Jonsson PR (1990) Foraging behavior of six calanoid copepods: observations and hydrodynamic analysis. Mar Ecol Prog Ser 66:23–33CrossRefGoogle Scholar
  62. Titelman J, Kiørboe T (2003) Motility of copepod nauplii and implications for food encounter. Mar Ecol Prog Ser 247:123–135CrossRefGoogle Scholar
  63. Turner JT, Tester PA (1989) Zooplankton feeding ecology: nonselective grazing by the copepods Acartia tonsa Dana, Centropages velificatus de Oliveira, and Eucalanus pileatus Giesbrecht in the plume of the Mississippi River. J Exp Mar Bio Ecol 126:21–43CrossRefGoogle Scholar
  64. Turner JT, Ianora A, Miralto A, Laabir M, Esposito F (2001) Decoupling of copepod grazing rates, fecundity and egg hatching success on mixed and alternating diatom and dinoflagellate diets. Mar Ecol Prog Ser 220:187–199CrossRefGoogle Scholar
  65. Verity P, Smayda TJ (1989) Nutritional value of Phaeocystis pouchetii (Prymnesiophyceae) and other phytoplankton for Acartia spp. (Copepoda): ingestion, egg production, and growth of nauplii. Mar Biol 100:161–171Google Scholar
  66. Vidoudez C, Pohnert G (2008) Growth phase-specific release of polyunsaturated aldehydes by the diatom Skeletonema marinoi. J Plankton Res 30:1305–1313CrossRefGoogle Scholar
  67. Vidoudez C, Nejstgaard JC, Jakobsen HH, Pohnert G (2011) Dynamics of dissolved and particulate polyunsaturated aldehydes in mesocosms inoculated with different densities of the diatom Skeletonema marinoi. Mar Drugs 9:500–513CrossRefGoogle Scholar
  68. Wichard T, Gerecht A, Boersma M, Poulet SA, Wiltshire K, Pohnert G (2007) Lipid and fatty acid composition of diatoms revisited: rapid wound-activated change of food quality parameters influences herbivorous copepod reproductive success. Chem BioChem 8:1146–1153Google Scholar
  69. Wichard T, Poulet SA, Bouleseix A-L, Ledoux JB, Lebreton B, Marchetti J, Pohnert G (2008) Influence of diatoms on copepod reproduction. II. Uncorrelated effects of diatom-derived α, β, γ, δ-unsaturated aldehydes and polyunsaturated fatty acids on Calanus helgolandicus in the field. Prog Oceanogr 77:30–44CrossRefGoogle Scholar
  70. Woodson CB, Webster DR, Weissburg MJ, Yen J (2005) Response of copepods to physical gradients associated with structure in the ocean. Limnol Oceangr 50:1552–1564CrossRefGoogle Scholar

Copyright information

© The Author(s) 2011

Open AccessThis is an open access article distributed under the terms of the Creative Commons Attribution Noncommercial License (, which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.

Authors and Affiliations

  • Roswati Md Amin
    • 1
    • 2
    • 3
  • Marja Koski
    • 4
  • Ulf Båmstedt
    • 1
    • 2
  • Charles Vidoudez
    • 5
  1. 1.Umeå Marine Sciences CentreUmeå UniversityHörneforsSweden
  2. 2.Department of Ecology and Environmental SciencesUmeå UniversityUmeåSweden
  3. 3.Department of Marine Science, Faculty of Maritime Studies and Marine ScienceUniversiti Malaysia TerengganuKualaMalaysia
  4. 4.National Institute of Aquatic ResourcesTechnical University of DenmarkCharlettenlundDenmark
  5. 5.Departement of organismic and evolutionary biologyHarvard UniversityCambridgeUSA

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