Marine Biology

, Volume 156, Issue 3, pp 469–477 | Cite as

Increased production of faecal pellets by the benthic harpacticoid Paramphiascella fulvofasciata: importance of the food source

  • Marleen De Troch
  • Clio Cnudde
  • Wim Vyverman
  • Ann Vanreusel
Original Paper

Abstract

The re-use of faecal pellets in the water column before sinking to the seafloor is known as an important pathway in marine food webs. Especially planktonic copepods seems to be actively use their faecal pellets. Since benthic copepods (order Harpacticoida) live in the vicinity of their pellets, it remains unclear how important these pellets are for their feeding ecology. In the present study a laboratory experiment was conducted to analyse the importance of faecal pellets for the feeding ecology of the harpacticoid Paramphiascella fulvofasciata and its grazing pressure on two diatom species (Seminavis robusta, Navicula phyllepta). By quantifying the amount and volume of the produced faecel pellets in different treatments, it was tested to what extent the food source and the lack of faecal pellets would influence the production of faecal pellets. We found that the grazing pressure of P. fulvofasciata depended on the diatom density since only a top-down effect could be found on the smaller Navicula cells during its initial exponential growth phase. The grazer had a negative effect on the diatom growth and controlled the cell density to about 4,000 cells/cm2. In spite of the fact that the addition of faecal pellets did not show a significant positive effect on the assimilation of diatoms, the removal of faecal pellets strongly promoted the pellet production. Especially when grazing on Navicula the harpacticoid P. fulvofasciata produced significantly more and smaller faecal pellets when the pellets were removed. This outcome illustrates the need for faecal pellets of this harpacticoid copepod when grazing on the diatom Navicula. Apart from its selection for smaller diatom cells, it was suggested that the colonisation of heterotrophic bacteria enriched these pellets. This study is the first to indicate that trophic upgrading occurs on faecal pellets and not only on the initial autotrophic food sources per se.

Keywords

Faecal Pellet Navicula Harpacticoid Copepod Diatom Cell Planktonic Copepod 

Notes

Acknowledgments

M. de Troch is a Postdoctoral Fellow of the Research Foundation - Flanders (FWO). This study was conducted within the frame of FWO research project G.0313.04. Additional support was provided by the Ghent University (BOF-GOA 01GZ0705). The authors acknowledge the support by the MarBEF Network of Excellence ‘Marine Biodiversity and Ecosystem Functioning’ which is funded by the Sustainable Development, Global Change and Ecosystems Programme of the European Community’s Sixth Framework Programme (contract no. GOCE-CT-2003-505446). This publication is contribution MPS-08049 of MarBEF. Two anonymous referees provided valuable remarks in order to improve an earlier version of this paper.

References

  1. Araújo-Castro CMV, Souza-Santos LP (2005) Are the diatoms Navicula sp. and Thalassiosira fluviatilis suitable to be fed to the benthic harpacticoid copepod Tisbe biminiensis?. J Exp Mar Biol Ecol 327:58–69. doi: 10.1016/j.jembe.2005.06.005 CrossRefGoogle Scholar
  2. Bec A, Martin-Creuzburg D, von Elert E (2006) Trophic upgrading of autotrophic picoplankton by the heterotrophic nanoflagellate Paraphysomonas sp. Limnol Oceanogr 51:1699–1707Google Scholar
  3. Chepurnov VA, Mann DG, Vyverman W, Sabbe K, Danielidis DB (2002) Sexual reproduction, mating system, and protoplast dynamics of Seminavis (Bacillariophyta). J Phycol 38:1004–1019. doi: 10.1046/j.1529-8817.2002.t01-1-01233.x CrossRefGoogle Scholar
  4. Cowey CB, Corner ED (1966) The amino acid composition of certain unicellular algae, and of the fecal pellets produced by Calanus jinmurchicus when feeding on them. In: Barnes H (ed) Some contemporary studies in marine science. Allen and Unwin, London, pp 225–231Google Scholar
  5. De Troch M, Steinarsdóttir MB, Chepurnov V, Ólafsson E (2005) Grazing on diatoms by harpacticoid copepods: species-specific density-dependent assimilation and microbial gardening. Aquat Microb Ecol 39:135–144. doi: 10.3354/ame039135 CrossRefGoogle Scholar
  6. De Troch M, Chepurnov V, Gheerardyn H, Vanreusel A, Ólafsson E (2006a) Is diatom size selection by harpacticoid copepods related to grazer body size? J Exp Mar Biol Ecol 332:1–11. doi: 10.1016/j.jembe.2005.10.017 CrossRefGoogle Scholar
  7. De Troch M, Houthoofd L, Chepurnov V, Vanreusel A (2006b) Does sediment grain size affect diatom grazing by harpacticoid copepods? Mar Environ Res 61:265–277. doi: 10.1016/j.marenvres.2005.10.004 PubMedCrossRefGoogle Scholar
  8. De Troch M, Grego M, Chepurnov VA, Vincx M (2007) Food patch size, food concentration and grazing efficiency of the harpacticoid Paramphiascella fulvofasciata (Crustacea, Copepoda). J Exp Mar Biol Ecol 343:210–216. doi: 10.1016/j.jembe.2006.12.022 CrossRefGoogle Scholar
  9. Feller RJ (1980) Development of the sand-dwelling meiobenthic harpacticoid copepod Hunternannia jadensis Poppe in the laboratory. J Exp Mar Biol Ecol 46:l–l15. doi: 10.1016/0022-0981(80)90086-6 CrossRefGoogle Scholar
  10. Gauld DT (1957) A peritrophic membrane in calanoid copepods. Nature 179:325–326. doi: 10.1038/179325a0 CrossRefGoogle Scholar
  11. Greenhouse SW, Geisser S (1959) On methods in the analysis of profile data. Psychometrika 24:95–112. doi: 10.1007/BF02289823 CrossRefGoogle Scholar
  12. Guillard RL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chandley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York, pp 26–60Google Scholar
  13. Decho AW, Fleeger JW (1988) Ontogenetic shifts in the meiobenthic harpacticoid copepod Nitocra lacustris. Mar Biol (Berl) 97:191–197. doi: 10.1007/BF00391302 CrossRefGoogle Scholar
  14. Hutchins DA, Wang WX, Fisher NS (1995) Copepod grazing and the biogeochemical fate of diatom iron. Limnol Oceanogr 40:989–994Google Scholar
  15. Huynh H, Feldt LS (1970) Conditions under which mean square ratios in repeated measures designs have exact F-distributions. J Am Stat Assoc 65:1582–1589. doi: 10.2307/2284340 CrossRefGoogle Scholar
  16. Jansen S, Bathmann U (2007) Algae viability within copepod faecal pellets: evidence from microscopic examinations. Mar Ecol Prog Ser 337:145–153. doi: 10.3354/meps337145 CrossRefGoogle Scholar
  17. Karrh RR, Miller DC (1994) Functional response of a surface-deposit feeder, Saccoglossus kowalevskii. Limnol Oceanogr 39:1455–1464CrossRefGoogle Scholar
  18. 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 (Berl) 135:191–198. doi: 10.1007/s002270050616 CrossRefGoogle Scholar
  19. Liu S, Wang W-X, Huang L-M (2006) Phosphorus dietary assimilation and efflux in the marine copepod Acartia erythraea. Mar Ecol Prog Ser 321:193–202CrossRefGoogle Scholar
  20. Miller CA, Roman MR (2008) Effects of food nitrogen content and concentration on the forms of nitrogen excreted by the calanoid copepod, Acartia tonsa. J Exp Mar Biol Ecol 359:11–17. doi: 10.1016/j.jembe.2008.02.016 CrossRefGoogle Scholar
  21. Moens T, Van Gansbeke D, Vincx M (1999) Linking estuarine nematodes to their suspected food. A case study from the Westerschelde Estuary (south-west Netherlands). J Mar Biol Assoc U K 79:1017–1027. doi: 10.1017/S0025315499001253 CrossRefGoogle Scholar
  22. Mourelatos S, Rougier C, Lacroix G (1992) Radiotracer losses due to freezing in formalin of carbon-14-labeled cladocerans. Arch Hydrobiol 126:239–253Google Scholar
  23. Noji TT, Estep KW, Macintyre F, Norrbin F (1991) Image-analysis of fecal material grazed upon by 3 species of copepods—evidence for coprorehxy, coprophagy and coprochaly. J Mar Biol Assoc UK 71:465–480CrossRefGoogle Scholar
  24. Paffenhöffer GA, Van Sant KB (1985) The feeding response of a marine planktonic copepod to quantity and quality of particles. Mar Ecol Prog Ser 27:55–65. doi: 10.3354/meps027055 CrossRefGoogle Scholar
  25. Reigstad M, Wexels Riser C, Svensen C (2005) Fate of copepod faecal pellets and the role of Oithona spp. Mar Ecol Prog Ser 304:265–270. doi: 10.3354/meps304265 CrossRefGoogle Scholar
  26. Reinfelder JR, Fisher NS (1991) The assimilation of elements ingested by marine copepods. Science 215:794–796. doi: 10.1126/science.251.4995.794 CrossRefGoogle Scholar
  27. Tang KW, Taal M (2005) Trophic modification of food quality by heterotrophic protists: species-specific effects on copepod egg production and egg hatching. J Exp Mar Biol Ecol 318:85–98. doi: 10.1016/j.jembe.2004.12.004 CrossRefGoogle Scholar
  28. Thor P, Koski M, Tang K, Jonasdottir SH (2007) Supplemental effects of diet mixing on absorption of ingested organic carbon in the marine copepod Acartia tonsa. Mar Ecol Prog Ser 331:131–138CrossRefGoogle Scholar
  29. Turner JY (2002) Zooplankton fecal pellets, marine snow and sinking phytoplankton blooms. Aquat Microb Ecol 27:57–102. doi: 10.3354/ame027057 CrossRefGoogle Scholar
  30. Viitasalo M, Rosenberg M, Heiskanen AS, Koski M (1999) Sedimentation of copepod fecal material in the coastal northern Balthic Sea: where did all the pellets go? Limnol Oceanogr 44:1388–1399Google Scholar
  31. Walker I (1979) Mechanisms of density-dependent population regulation in the marine copepod Amphiascoides sp. (Harpacticoida). Mar Ecol Prog Ser 1:209–221. doi: 10.3354/meps001209 CrossRefGoogle Scholar
  32. Wexels Riser C, Reigstad M, Wassmann P, Arashkevich E, Falk-Petersen S (2007) Export or retention? Copepod abundance, faecal pellet production and vertical flux in the marginal ice zone through snap shots from the northern Barents Sea. Polar Biol 30:719–730. doi: 10.1007/s00300-006-0229-z CrossRefGoogle Scholar
  33. Wotton RS (2001) Life in water. An internet book. Chapter 5: Trophic status, food availability and feeding by aquatic animals. http://www.ucl.ac.uk/~ucbt212/

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Marleen De Troch
    • 1
  • Clio Cnudde
    • 1
  • Wim Vyverman
    • 2
  • Ann Vanreusel
    • 1
  1. 1.Biology Department, Marine BiologyGhent UniversityGhentBelgium
  2. 2.Biology Department, Protistology and Aquatic EcologyGhent UniversityGhentBelgium

Personalised recommendations