Marine Biology

, 165:25 | Cite as

First genetic quantification of sex- and stage-specific feeding in the ubiquitous copepod Acartia tonsa

  • Stefanie M. H. Ismar
  • Johanna S. Kottmann
  • Ulrich Sommer
Original paper


Marine copepods provide the major food-web link between primary producers and higher trophic levels, and their feeding ecology is of acute interest in light of global change impacts on food-web functioning. Recently, quantitative polymerase chain reaction (qPCR) protocols have been developed, which can complement classic diet quantification methods, such as stable isotope or fatty acid analyses tools. Here, we present first results of feeding experiments assessing sex- and stage-specific food intake by the ubiquitous calanoid copepod Acartia tonsa by 18S targeted qPCR and microscopic grazing assessment. In triplicated mixed-diet feeding treatments, three suitable A. tonsa diets, the cryptophyte Rhodomonas balthica, the haptophyte Isochrysis galbana, and the diatom Thalassiosira weissflogii, were offered in equal biomass proportions under constant conditions. Prey uptake substantially varied between different algal species, as did the extent of sex- and stage-specificity of prey uptake. Male adult copepods had higher R. balthica gut contents than females, and nauplii contained more of this prey source than copepodites or adult copepods in mixed treatments. A trend towards higher amounts of ingested T. weissflogii in adult females than in males and in nauplii than in other stages was detected. Genetic gut content quantifications indicated low feeding on I. galbana, and no consistent sex- or stage-specific differences of I. galbana content in A. tonsa. Our results highlight diet-specific feeding differences between Acartia life stages and sexes, which can have implications on food-web dynamics and specific nutrient transfer to higher trophic levels in copepod populations of varying age composition under changing environmental parameters, such as rising temperatures and increasing ocean acidification.



We thank K. Beining for helpful technical advice on real-time PCR, R. Nakad for advice on primer design, D. Riemann for Utermöhl counts of prey cell abundances, and two anonymous referees for helpful revision of our manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest. No vertebrate or invertebrate animals falling under ethical protection regulations were involved in the experiments by any of the authors.

Supplementary material

227_2017_3281_MOESM1_ESM.pdf (798 kb)
Supplementary material 1 (PDF 798 kb)
227_2017_3281_MOESM2_ESM.pdf (599 kb)
Supplementary material 2 (PDF 598 kb)
227_2017_3281_MOESM3_ESM.pdf (487 kb)
Supplementary material 3 (PDF 487 kb)


  1. Barofsky A, Simonelli P, Vidoudez C, Troedsson C, Nejstgaard JC, Jakobsen HH, Pohnert G (2010) Growth phase of the diatom Skeletonema marinoi influences the metabolic profile of the cells and the selective feeding of the copepod Calanus spp. J Plankton Res 32(3):262–273CrossRefGoogle Scholar
  2. Behrends G (1996) Long-term investigation of seasonal mesozooplankton dynamics in Kiel Bight, Germany. In: Proc. 13th Baltic Marine biology symposium, Jurmala, Latvia. Inst. Aquatic Ecology, University of Latvia, Riga, Latvia, pp 93–98Google Scholar
  3. Blankenship LE, Yayanos AA (2005) Universal primers and PCR of gut contents to study marine invertebrate diets. Mol Ecol 14:891–899CrossRefGoogle Scholar
  4. Boersma M, Wesche A, Hirche HJ (2014) Predation of calanoid copepods on their own and other copepods’ offspring. Mar Biol 161:733–743CrossRefGoogle Scholar
  5. Broglio E, Jónasdóttir SH, Calbet A, Jakobsen HH, Saiz E (2003) Effect of heterotrophic food on feeding and reproduction of the calanoid copepod Acartia tonsa: relationship with prey fatty acid composition. Aquat Microb Ecol 31:267–278CrossRefGoogle Scholar
  6. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE Guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55(4):611–622CrossRefGoogle Scholar
  7. Cervetto G, Pagano M, Gaudy R (1995) Feeding behavior and migrations in a natural population of the copepod Acartia tonsa. Hydrobiologia 300:237–248CrossRefGoogle Scholar
  8. Conroy BJ, Steinberg DK, Song B, Kalmbach A, Carpenter EJ, Foster RA (2017) Mesozooplankton graze on cyanobacteria in the Amazon River Plume and Western Tropical North Atlantic. Front Microbiol. Google Scholar
  9. Cushing DH (1990) Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Adv Mar Biol 26:249–293CrossRefGoogle Scholar
  10. Dassow P, Petersen TW, Chepumov VA, Armbrust EV (2008) Inter- and intraspecific relationships between nuclear DNA content and cell size in selected members of the centric diatom genus Thalassiosira (Bacillariophyceae). J Phycol 44:335–349CrossRefGoogle Scholar
  11. Durbin EG, Casas MC, Rynearson TA (2012) Copepod feeding and digestion rates using prey DNA and qPCR. J Plankton Res 34(1):72–82CrossRefGoogle Scholar
  12. Edwards M, Richardson AJ (2004) Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430:881–884CrossRefGoogle Scholar
  13. Eiane K, Ohman MD (2004) Stage-specific mortality of Calanus finmarchicus, Pseudocalanus elongatus and Oithona similis on Fladen Ground, North Sea, during a spring bloom. Mar Ecol Progr Ser 268:183–193CrossRefGoogle Scholar
  14. Frost BW (1972) Effects of size and concentrations of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnol Oceanogr 14:805–815CrossRefGoogle Scholar
  15. Garzke J, Ismar SMH, Sommer U (2015) Climate change affects low trophic level marine consumers: warming decreases copepod size and abundance. Oecologia 177:849–860CrossRefGoogle Scholar
  16. Garzke J, Hansen T, Ismar SMH, Sommer U (2016) Combined effects of ocean warming and acidification on copepod abundance, body size and fatty acid content. PLoS ONE 11:e0155952CrossRefGoogle Scholar
  17. Garzke J, Sommer U, Ismar SMH (2017) Is the chemical composition of biomass the agent by which ocean acidification impacts on zooplankton ecology? Aquat Sci 79:233–249CrossRefGoogle Scholar
  18. Giesecke R, Vallejos T, Sanchez M, Teiguiel K (2017) Plankton dynamics and zooplankton carcasses in a mid-latitude estuary and their contributions to the local particulate organic carbon pool. Cont Shelf Res 132:58–68CrossRefGoogle Scholar
  19. Hansen FC, Möllmann C, Schütz U, Neumann T (2006) Spatio-temporal distribution and production of calanoid copepods in the central Baltic Sea. J Plankton Res 28(1):39–54CrossRefGoogle Scholar
  20. Harper GL, King RA, Dodd CS, Harwood JD, Glen DM, Bruford MW, Symondson WOC (2005) Rapid screening of invertebrate predators for multiple prey DNA targets. Mol Ecol 14:819–827CrossRefGoogle Scholar
  21. Helenius LK, Saiz E (2017) Feeding behavior of the marine calanoid copepod Paracartia grani Sars: functional response, prey size spectrum, and effects of the presence of alternative prey. PLoS ONE 12(3):e0172902CrossRefGoogle Scholar
  22. Hillebrand H, Dürselen C-D, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424CrossRefGoogle Scholar
  23. Hu S, Gao Z, Xu C, Huang H, Liu S, Lin S (2015) Molecular analysis on in situ diets of coral reef copepods: evidence of terrestrial plant detritus as a food source in Anya Bay, China. J Plankton Res 37(2):363–371CrossRefGoogle Scholar
  24. IPCC (2014) Climate Change 2014: mitigation of climate change. Contribution of Working Group III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, New YorkGoogle Scholar
  25. Isari S, Antό M, Saiz E (2013) Copepod foraging on the basis of food nutritional quality: can copepods really choose? PLoS ONE 8:e84742CrossRefGoogle Scholar
  26. Ismar SMH, Hansen T, Sommer U (2008) Effect of food concentration and type of diet on Acartia survival and naupliar development. Mar Biol 154:335–343CrossRefGoogle Scholar
  27. Jager T, Slaberria I, Altin D, Nordtug T, Hansen BH (2017) Modelling the dynamics of growth, development and lipid storage in the marine copepod Calanus finmarchicus. Mar Biol 164(1):1CrossRefGoogle Scholar
  28. Jonsson PR, Tiselius P (1990) Feeding behaviour, prey detection and capture efficiency of the copepod Acartia tonsa feeding on planktonic ciliates. Mar Ecol Progr Ser 60:35–44CrossRefGoogle Scholar
  29. Jungbluth MJ, Goetze E, Lenz PH (2013) Measuring copepod naupliar abundance in a subtropical bay using quantitative PCR. Mar Biol 160:3125–3141CrossRefGoogle Scholar
  30. Jungbluth MJ, Selph KE, Lenz PH, Goetze E (2017) Species-specific and significant trophic impacts by two species of copepod nauplii, Parvocalanus crassirostris and Bestiolina similis. Mar Ecol Prog Ser 572:57–76CrossRefGoogle Scholar
  31. Kawabata K (1991) Ontogenetic changes in copepod behavior—an ambush cyclopoid predator and a calanoid prey. J Plankton Res 13(1):27–34CrossRefGoogle Scholar
  32. Kiørboe T (1998) Population regulation and role of mesozooplankton in shaping marine pelagic food webs. In: Tamminen T, Kuosa H (eds) Eutrophication in planktonic ecosystems: food web dynamics and elemental cycling. Springer, Netherlands, pp 13–27CrossRefGoogle Scholar
  33. Kiørboe T (2008) Optimal swimming strategies in mate searching pelagic copepods. Oecologia 155:179–192CrossRefGoogle Scholar
  34. Kiørboe T (2011) What makes pelagic copepods so successful? J Plankton Res 33:677–685CrossRefGoogle Scholar
  35. Kiørboe T, Bagøien E (2005) Motility patterns and mate encounter rates in planktonic copepods. Limnol Oceanogr 50:1999–2007CrossRefGoogle Scholar
  36. Kiørboe T, Ceballos S, Thygesen UH (2015) Interrelations between senescence, life-history traits, and behavior in planktonic copepods. Ecology 96(8):2225–2235CrossRefGoogle Scholar
  37. Knuckey RM, Semmens GL, Mayer RJ, Rimmer MA (2005) Development of an optimal microalgal diet for the culture of the calanoid copepod Acartia sinjiensis: effect of algal species and feed concentration on copepod development. Aquaculture 249:339–351CrossRefGoogle Scholar
  38. Lewandowska AM, Boyce DG, Hofmann M, Matthiessen B, Sommer U, Worm B (2014) Effects of sea surface warming on marine plankton. Ecol Lett 17(5):614–623CrossRefGoogle Scholar
  39. Lund JWG, Kipling C, LeCren ED (1958) The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11:143–170CrossRefGoogle Scholar
  40. Mauchline J (1998) The biology of calanoid copepods. In: Blaxter JHS, Southward AJ, Tyler PA (eds) Advances in marine biology 33. Academic Press, New York, pp 1–710Google Scholar
  41. Menden-Deuer S, Lessard EJ (2000) Carbon to volume relationships for dinoflagellates, diatoms, and of the protist plankton. Limnol Oceanogr 45:559–579CrossRefGoogle Scholar
  42. Meunier CL, Boersma M, Wiltshire K, Malzahn AM (2016) Zooplankton eat what they need: copepod selective feeding and potential consequences for marine systems. Oikos 125:50–58CrossRefGoogle Scholar
  43. Milione M, Zeng C (2007) The effects of algal diets on population growth and egg hatching success of the tropical calanoid copepod, Acartia sinjiensis. Aquaculture 273(4):656–664CrossRefGoogle Scholar
  44. Möllmann C, Kornilovs G, Fetter M, Köster FW (2005) Climate, zooplankton, and pelagic fish growth in the central Baltic Sea. ICES J Mar Sci 62:1270–1280CrossRefGoogle Scholar
  45. Moorthi SD, Countway PD, Stauffer BA, Caron DA (2006) Use of quantitative real-time PCR to investigate the dynamics of the red tide dinoflagellate Lingulodinium polyedrum. Micr Ecol 52:135–150Google Scholar
  46. Nejstgaard JC, Frischer ME, Raule CL, Gruebel R, Kohlberg KE, Verity PG (2003) Molecular detection of algal prey in copepod guts and fecal pellets. Limnol Oceanogr Methods 1:29–38CrossRefGoogle Scholar
  47. Nejstgaard JC, Frischer ME, Simonelli P, Troedsson C, Brakel M, Adiyaman F, Sazhin AF, Artigas LF (2008) Quantitative PCR to estimate copepod feeding. Mar Biol 153:565–577CrossRefGoogle Scholar
  48. Pan YJ, Souissi A, Souissi S, Hwang JS (2016) Effects of salinity on the reproductive performance of Apocyclops royi (Copepoda, Cyclopoida). J Exp Mar Biol Ecol 475:108–113CrossRefGoogle Scholar
  49. Rayner TA, Jørgensen NO, Drillet G, Hansen BW (2017) Changes in free amino acid content during naupliar development of the Calanoid copepod Acartia tonsa. Comp Biochem Physiol A 210:1–6CrossRefGoogle Scholar
  50. Saiz E, Calbet A (2011) Copepod feeding in the ocean: scaling patterns, composition of their diet and the bias of estimates due to microzooplankton grazing during incubations. Hydrobiologia 666:181–196CrossRefGoogle Scholar
  51. Saiz E, Calbet A, Stamatina I (2014) Feeding rates and prey: predator size ratios of the nauplii and adult females of the marine cyclopoid Oithona davisae. Limnol Oceanogr 59(6):2077–2088CrossRefGoogle Scholar
  52. Shayegan M, Esmaeili FA, Agh N, Jani KK (2016) Effects of salinity on egg and fecal pellet production, development and survival, adult sex ratio and life span in the calanoid copepod Acartia tonsa: a laboratory study. Chin J Oceanol Limnol 34:709–718CrossRefGoogle Scholar
  53. Sheppard SK, Harwood JD (2005) Advances in molecular ecology: tracking trophic links through predator-prey food-webs. Funct Ecol 19:751–762CrossRefGoogle Scholar
  54. Simonelli P, Troedsson C, Nejstgaard JC, Zech K, Larsen JB, Frischer ME (2009) Evaluation of DNA extraction and handling procedures for PCR-based copepod feeding studies. J Plankton Res 31:1465–1474CrossRefGoogle Scholar
  55. Smith KF, Biessy L, Argyle PA, Trnski T, Halafihi T, Rhodes LL (2017) Molecular identification of Gambierdiscus and Fukuyoa (Dinophyceae) from environmental samples. Marine Drugs 15:243CrossRefGoogle Scholar
  56. Sommer U (2009) Copepod growth and diatoms: insensitivity of Acartia tonsa to the composition of semi-natural plankton mixtures manipulated by Si:N ratios in mesocosms. Oecologia 159:207–215CrossRefGoogle Scholar
  57. Sommer U, Lewandowska A (2011) Climate change and the phytoplankton spring bloom: warming and overwintering zooplankton have similar effects on phytoplankton. Glob Change Biol 17:154–162CrossRefGoogle Scholar
  58. Sommer U, Stibor H, Katechakis A, Sommer F, Hansen T (2002) Pelagic food web configuration at different levels of nutrient richness and their implications for the ratio fish production: primary production. Hydrobiologia 484:110–120CrossRefGoogle Scholar
  59. Sommer F, Saage A, Santer B, Hansen T, Sommer U (2005) Linking foraging strategies of marine calanoid copepods to patterns of nitrogen stable isotope signatures in a mesocosm study. Mar Ecol Prog Ser 286:99–106CrossRefGoogle Scholar
  60. Støttrup JG, Jensen J (1990) Influence of algal diet on feeding and egg-production of the calanoid copepod Arcatia tonsa Dana. J Exp Mar Biol Ecol 141:87–105CrossRefGoogle Scholar
  61. Støttrup JG, Richardson K, Kirkegaard E, Pihl NG (1986) The cultivation pf Acartia tonsa Dana for use as live food for marine fish larvae. Aquaculture 52(2):87–96CrossRefGoogle Scholar
  62. Troedsson C, Frischer ME, Nejstgaard JC, Thompson EM (2007) Molecular quantification of differential ingestion and particle trapping rates by the appendicularian Oikopleura dioica as a function of prey size and shape. Limnol Oceanogr 52:416–427CrossRefGoogle Scholar
  63. Troedsson C, Simonelli P, Nägele V, Nejstgaard JC, Frischer ME (2009) Quantification of copepod gut content by differential length amplification quantitative PCR (dla-qPCR). Mar Biol 156:253–259CrossRefGoogle Scholar
  64. Utermöhl (1958) Zur Vervollkommnung der quantitativen Phytoplankton Methodik. Mitt Int Ver Theor Angew Limnol 9:263–272Google Scholar
  65. Van Duren LA, Videler JJ (1996) The trade-off between feeding, mate seeking and predator avoidance in copepods: Behavioural responses to chemical cues. J Plankton Res 18(5):805–818CrossRefGoogle Scholar
  66. Zervoudaki S, Krasakopoulou E, Moutsopoulos T, Protopapa M, Marro S, Gazeau F (2017) Copepod response to ocean acidification in a low nutrient-low chlorophyll environment in the NW Mediterranean Sea. Est Coast Shelf Sci 186:152–162CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Stefanie M. H. Ismar
    • 1
  • Johanna S. Kottmann
    • 1
    • 2
  • Ulrich Sommer
    • 1
  1. 1.GEOMAR Helmholtz Center for Ocean Research KielMarine EcologyKielGermany
  2. 2.National Institute of Aquatic ResourcesTechnical University of DenmarkCharlottenlundDenmark

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