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Marine Biology

, Volume 150, Issue 2, pp 221–235 | Cite as

Trophic impact, metabolism, and biogeochemical role of the marine cladoceran Penilia avirostris and the co-dominant copepod Oithona nana in NW Mediterranean coastal waters

  • Dacha Atienza
  • Albert Calbet
  • Enric Saiz
  • Miquel Alcaraz
  • Isabel Trepat
Research Article

Abstract

In this work we studied the trophic ecology and feeding impact of the cladoceran Penilia avirostris and the cyclopoid copepod Oithona nana, the two dominant zooplankters in the summer communities of the coastal NW Mediterranean, on the naturally occurring microbial communities. In order to ascertain carbon surplus for growth and reproduction and the contribution to carbon and nitrogen recycling of these two species, we also determined their basal metabolism and excretion rates. The experiments conducted during summers 2002, 2003, and 2004 indicate that P. avirostris grazed mostly upon small flagellates, dinoflagellates, and diatoms, whereas O. nana had a narrower prey range, selecting motile organisms such as ciliates and occasionally dinoflagellates. The grazing impact of both species accounted, on average, for <10% of the standing stock of the microbial groups considered. In spite of the oligotrophic conditions, the feeding activity of P. avirostris is in general sufficient to compensate basal metabolism and allows a surplus for growth and reproduction. This was not the case for O. nana, its daily rations being often lower than the carbon basal demands. Regarding excretion rates, both species presented different N:P excretion ratios, the ones of O. nana falling within values typical for copepods, whereas the absence of detectable phosphorus excretion by P. avirostris implied an unbalance recycling with respect to typical Redfield ratio composition of marine seston.

Keywords

Dinoflagellate Clearance Rate Excretion Ratio Standing Stock Prochlorococcus 
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.

Notes

Acknowledgements

This work was supported by a PhD fellowship from the Spanish Government to D.A., by the Spanish CICYT projects REN2001-1693 to E.S., and CTM2004-02575/MAR and Program Ramón y Cajal from the Ministry of Education and Science of Spain to A.C. We also want to thank the help of the Captain and crew of the Harbour of Masnou, and Pepito and Ramón who kindly provided facilities and access to the sea. Finally, we want to thank Belén Aguilera for her inestimable help counting the samples, and four anonymous reviewers for their constructive comments on the manuscript.

References

  1. Alcaraz M (1970) Ciclo anual de los cladóceros en aguas de Castellón (Mediterráneo occidental). Inv Pesq 34:281–290Google Scholar
  2. Alcaraz M (1981) Ciclo anual de los cladóceros y ostrácodos planctónicos en la plataforma continental de Vizcaya (Punta Endata). Inv Pesq 45:3–16Google Scholar
  3. Andersen T, Elser JJ, Hessen DO (2004) Stoichiometry and population dynamics. Ecol Lett 7:884–900CrossRefGoogle Scholar
  4. Atienza D, Saiz E, Calbet A (2006) Feeding ecology of the marine cladoceran Penilia avirostris. Natural diets, daily ration and prey selectivity. Mar Ecol Prog Ser (in press)Google Scholar
  5. Båmstedt U, Gifford DJ, Irigoien X, Atkinson A, Roman M, Harris RP (2000) Feeding. In: Wiebe PH, Lenz J, Skjoldal HR, Huntley M (eds) ICES Zooplankton Methodology Manual. Academic, UK, pp 297–399Google Scholar
  6. Berggren U, Hansen B, Kiorboe T (1988) Food size spectra, ingestion and growth of the copepod Acartia tonsa during development: implications for determination of copepod production. Mar Biol 99:341–352CrossRefGoogle Scholar
  7. Børsheim KY, Bratbak G (1987) Cell volume to cell carbon conversion factors for a bacterivorous Monas sp. enriched from seawater. Mar Ecol Prog Ser 36:171–175CrossRefGoogle Scholar
  8. Broglio E, Saiz E, Calbet A, Trepat I, Alcaraz M (2004) Trophic impact and prey selection by crustacean zooplankton on the microbial communities of an oligotrophic coastal area (NW Mediterranean Sea). Aquat Microb Ecol 35:65–78CrossRefGoogle Scholar
  9. Calbet A, Saiz E (2005) The ciliate–copepod link in marine ecosystems. Aquat Microb Ecol 38:157–167CrossRefGoogle Scholar
  10. Calbet A, Landry MR, Scheinberg RD (2000) Copepod grazing in a subtropical bay: species-specific responses to a midsummer increase in nanoplankton standing stock. Mar Ecol Prog Ser 193:75–84CrossRefGoogle Scholar
  11. Calbet A, Garrido S, Saiz E, Alcaraz M, Duarte M (2001) Annual zooplankton succession in coastal NW Mediterranean waters: the importance of the smaller size fractions. J Plankton Res 23:319–331CrossRefGoogle Scholar
  12. Carrillo P, Reche I, Cruz-Pizarro L (1996) Intraspecific stoichiometric variability and the ratio of nitrogen to phosphorus resupplied by zooplankton. Freshw Biol 36:363–374CrossRefGoogle Scholar
  13. Castellani C, Robinson C, Smith T, Lampitt RS (2005) Temperature affects respiration rate of Oithona similis. Mar Ecol Prog Ser 285:129–135CrossRefGoogle Scholar
  14. Christou ED, Moraitou-Apostopoulou M (1995) Metabolism and feeding of mesozooplankton in the Eastern Mediterranean (Hellenic coastal waters). Mar Ecol Prog Ser 126:39–48CrossRefGoogle Scholar
  15. Debs CA (1984) Carbon and nitrogen budget of the calanoid copepod Temora stylifera: effect of concentration and composition of food. Mar Ecol Prog Ser 15:213–223CrossRefGoogle Scholar
  16. Egloff DA, Fofonoff PW, Onbé T (1997) Reproductive biology of marine cladocerans. Adv Mar Biol 31:79–168CrossRefGoogle Scholar
  17. Elser JJ, Urabe J (1999) The stoichiometry of consumer-driven nutrient cycling: theory, observations, and consequences. Ecology 80:735–751CrossRefGoogle Scholar
  18. Elser JJ, Elser MM, MacKay NA, Carpenter SR (1988) Zooplankton-mediated transitions between N- and P- limited algal growth. Limnol Oceanogr 33:1–14CrossRefGoogle Scholar
  19. Elser JJ, Dobberfuhl DR, MacKay NA, Schampel JH (1996) Organism size, life history, and N:P stoichiometry: toward a unified view of cellular and ecosystem processes. BioScience 46:674–684CrossRefGoogle Scholar
  20. Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB, Harrison JF, Hobbie SE, Odell GM, Weider LJ (2000) Biological stoichiometry from genes to ecosystems. Ecol Lett 3:540–550CrossRefGoogle Scholar
  21. Frangoulis C, Christou ED, Hecq JH (2005) Comparison of marine copepod outfluxes: nature, rate, fate and role in the carbon and nitrogen cycles. Adv Mar Biol 47:254–309Google Scholar
  22. 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
  23. Gabriel W, Thomas B (1988) Vertical migration of zooplankton as an evolutionarily stable strategy. Am Nat 132:199–216CrossRefGoogle Scholar
  24. Gaudy R, Boucher J (1983) Relation between respiration, excretion (ammonia and inorganic phosphorus) and activity of amylase and trypsin in different species of pelagic copepods from an Indian Ocean equatorial area. Mar Biol 75:37–45CrossRefGoogle Scholar
  25. Gaudy R, Cervetto G, Pagano M (2000) Comparison of the metabolism of Acartia clausi and A. tonsa: influence of temperature and salinity. J Exp Mar Biol Ecol 247:51–65CrossRefGoogle Scholar
  26. Gismervik I (1997) Stoichiometry of some marine plankton crustaceans. J Plankton Res 19(2):279–285CrossRefGoogle Scholar
  27. González HE, Smetacek V (1994) The possible role of the cyclopoid copepod Oithona in retarding vertical flux of zooplankton faecal material. Mar Ecol Prog Ser 113:233–246CrossRefGoogle Scholar
  28. Gore MA (1980) Feeding experiments on Penilia avirostris Dana (Cladocera: Crustacea). J Exp Mar Biol Ecol 44:253–260CrossRefGoogle Scholar
  29. Gulati RD, Perez Martinez C, Siewertsen K (1995) Zooplankton as a compound mineralizing and synthesizing system: phosphorus excretion. Hydrobiology 315:25–37CrossRefGoogle Scholar
  30. Hansen HP, Koroleff F (1999) Determination of nutrients. In: Grasshoff K, Kremling K, Ehrhardt M (eds) Methods of seawater analysis. Wiley-VCH, New York, 159–228CrossRefGoogle Scholar
  31. Hansen PJ, Bjørnsen PK, Hansen BW (1997) Zooplankton grazing and growth: scaling within the 2-2000-μm body size range. Limnol Oceanogr 42:687–704CrossRefGoogle Scholar
  32. Harris RP (1988) Interactions between diel vertical migratory behavior of marine zooplankton and the subsurface chlorophyll maximum. Bull Mar Sci 43(3):663–674Google Scholar
  33. Hiromi J (1994) Further studies on respiration of the small planktonic copepod Oithona davisae with special reference to the effect of feeding. Bull Col Agric Vet Med Nihon Univ 51:149–153Google Scholar
  34. Hiromi J, Ichihashi O (1995) Influence of starvation length on the phosphate excretion rate of small sized copepod Oithona davisae. Bull Coll Agric Vet Med Nihon Univ 52:119–121Google Scholar
  35. Hiromi J, Nagata T, Kadota S (1988) Respiration of the small planktonic copepod Oithona davisae at different temperatures. Bull Plankton Soc Jpn 35:143–148Google Scholar
  36. Hopcroft RR, Roff JC, Lombard D (1998) Production of tropical copepods in Kingston Harbour, Jamaica: the importance of small species. Mar Biol 130:593–604CrossRefGoogle Scholar
  37. Ikeda T, Kanno Y, Ozaki K, Shinada A (2001) Metabolic rates of epipelagic marine copepods as a function of body mass and temperature. Mar Biol 139:587–596CrossRefGoogle Scholar
  38. Katechakis A, Stibor H, Sommer U, Hansen T (2002) Changes in the phytoplankton community and microbial food web of Blanes Bay (Catalan Sea, NW Mediterranean) under prolonged grazing pressure by doliolids (Tunicata), cladocerans or copepods (Crustacea). Mar Ecol Prog Ser 234:55–69CrossRefGoogle Scholar
  39. Katechakis A, Stibor H, Sommer U, Hansen T (2004) Feeding selectivities and food niche separation of Acartia clausi, Penilia avirostris (Crustacea) and Doliolum denticulatum (Thaliacea) in Blanes Bay (Catalan Sea, NW Mediterranean). J Plankton Res 26:589–603CrossRefGoogle Scholar
  40. Kim WC, Lai-Chun C, Quingchao C (1994) Ecology of the marine cladoceranPenilia avirostris Dana in Tolo Harbour, Hong Kong. Acta Oceanol Sin 13:117–127Google Scholar
  41. Lampitt RS, Gamble JC (1982) Diet and respiration of the small planktonic marine copepod Oithona nana. Mar Biol 66:185–190CrossRefGoogle Scholar
  42. Lipej L, Mozetic P, Turk V, Malej A (1997) The trophic role of the marine cladoceran Penilia avirostris in the Gulf of Trieste. Hydrobiology 360:197–203CrossRefGoogle Scholar
  43. Lonsdale DJ, Caron DA, Dennett MR, Schaffner R (2000) Predation by Oithona spp. on protozooplankton in the Ross Sea, Antarctica. Deep Sea Res II 47:3273–3283CrossRefGoogle Scholar
  44. Macedo CF, Pinto-Coelho M (2000) Diel variations in respiration, excretion rates, and nutritional status of zooplankton from the Pampulha reservoir, Belo Horizonte, MG. J Exp Zool 286:671–682CrossRefGoogle Scholar
  45. Mayzaud P, Conover RJ (1988) O:N atomic ratio as a tool to describe zooplankton metabolism. Mar Ecol Prog Ser 45:289–302CrossRefGoogle Scholar
  46. Mayzaud P, Razouls S, Errhif A, Tirelli V, Labat JP (2002) Feeding, respiration and egg production rates of copepods during austral spring in the Indian sector of the Antarctic Ocean: role of the zooplankton community in carbon transformation. Deep Sea Res I 49:1027–1048CrossRefGoogle Scholar
  47. Miller CA, Landry MR (1984) Ingestion-independent rates of ammonium excretion by the copepod Calanus pacificus. Mar Biol 78:265–270CrossRefGoogle Scholar
  48. Morán XAG, Estrada M, Gasol JM, Pedrós-Alió C (2002) Dissolved primary production and the strength of phytoplankton-bacterioplankton coupling in contrasting marine regions. Microb Ecol 44:217–223CrossRefGoogle Scholar
  49. Nakamura Y, Turner JT (1997) Predation and respiration by the small cyclopoid copepod Oithona similis: how important is feeding on ciliates and heterotrophic flagellates? J Plankton Res 19:1275–1288CrossRefGoogle Scholar
  50. Norland S (1993) The relationship between biomass and volume of bacteria. In: Kemp PF, Sherr BF, Sherr EB, Cole JJ (eds) Handbook of methods in aquatic microbial ecology. Lewis Publisher, Florida, pp 303–307Google Scholar
  51. Olsen Y, Jensen A, Reinertsen H, Børshein KY, Heldal M, Langeland A (1986) Dependence of the rate of release of phosphorus by zooplankton on the P:C ratio in the food supply, as calculated by a recycling model. Limnol Oceanogr 31:34–44CrossRefGoogle Scholar
  52. Onbé T (1985) Seasonal fluctuations in the abundance of populations of marine cladocerans and their resting eggs in the Inland Sea of Japan. Mar Biol 87:83–88CrossRefGoogle Scholar
  53. Onbé T, Ikeda T (1995) Marine cladocerans in Toyama Bay, southern Japan Sea: seasonal occurrence and day–night vertical distributions. J Plankton Res 17(3):595–609CrossRefGoogle Scholar
  54. Paffenhöfer GA (1983) On the ecology of marine cyclopoid copepods (Crustacea, Copepoda). J Plankton Res 15:37–55CrossRefGoogle Scholar
  55. Paffenhöfer GA, Gardner WS (1984) Ammonium release by juveniles and adult females of the subtropical marine copepod Eucalanus pileatus. J Plankton Res 6:505–513CrossRefGoogle Scholar
  56. Paffenhöfer GA, Orcutt JD (1986) Feeding, growth and food conversion of the marine cladoceran Penilia avirostris. J Plankton Res 8:741–754CrossRefGoogle Scholar
  57. Parson TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, New York, 173 ppGoogle Scholar
  58. Pavlova EG (1967) Food requirements of the Black Sea cladoceran Penilia avirostris Dana, and how they are met. Fisheries Research Board of Canada Translation Series 908, p 31Google Scholar
  59. Pérez-Martínez C, Gulati RD (1999) Species-specific N and P release rates in Daphnia. Hydrobiology 391:147–155CrossRefGoogle Scholar
  60. Picard V, Lair N (2000) The influence of autotrophic and heterotrophic foods on the demography of Daphnia longispina under starved, semi-natural and enriched conditions. J Plankton Res 22:1925–1944CrossRefGoogle Scholar
  61. Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948CrossRefGoogle Scholar
  62. Saiz E, Calbet A (2006) Scaling of feeding in marine calanoid copepods. Limnol Oceanogr (submitted)Google Scholar
  63. Sterner RW (1990) The ratio of nitrogen to phosphorus resupplied by herbivores: zooplankton and the algal competitive arena. Am Nat 136:209–229CrossRefGoogle Scholar
  64. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princetown University Press, PrincetownGoogle Scholar
  65. Sterner RW, Elser JJ, Hessen DO (1992) Stoichiometric relationships among producers, consumers and nutrient cycling in pelagic ecosystems. Biogeochemistry 17:49–67CrossRefGoogle Scholar
  66. Svensen C, Kiorboe T (2000) Remote prey detection in Oithona similis: hydromechanical vs. chemical cues. J Plankton Res 22:1155–1166CrossRefGoogle Scholar
  67. Turner JT, Tester PA, Ferguson RL (1988) The marine cladoceran Penilia avirostris and the “microbial loop” of pelagic food webs. Limnol Oceanogr 33:245–255CrossRefGoogle Scholar
  68. Uye S (1982) Length–weight relationships of important zooplankton from the Inland Sea of Japan. J Oceanogr Soc Jpn 38:149–158CrossRefGoogle Scholar
  69. Vaqué D, Blough HA, Duarte CM (1997) Dynamics of ciliate abundance, biomass and community composition in an oligotrophic coastal environment (NW Mediterranean). Aquat Microb Ecol 12:71–83CrossRefGoogle Scholar
  70. Verity PG, Smetacek V (1996) Organism life cycles, predation, and the structure of marine pelagic ecosystems. Mar Ecol Prog Ser 130:277–293CrossRefGoogle Scholar
  71. Walve J, Larsson UL (1999) Carbon, nitrogen and phosphorus stoichiometry of crustacean zooplankton in the Baltic Sea: implications for nutrient recycling. J Plankton Res 21:2309–2321CrossRefGoogle Scholar
  72. Waterbury JB, Watson SW, Valois FW, Franks DG (1986) Biological and ecological characterization of the marine unicellular cyanobacterium Synechococcus. Can Bull Fish Aquat Sci 214:71–1201Google Scholar
  73. Wiltshire KH, Lampert W (1999) Urea excretion by Daphnia: a colony-inducing factor in Scenedesmus? Limnol Oceanogr 44:1894–1903CrossRefGoogle Scholar
  74. Wong CK, Chan ALC, Tang KW (1992) Natural ingestion rates and grazing of the marine cladoceran Penilia avirostris Dana in Tolo Harbour, Hong Kong. J Plankton Res 14:1757–1765CrossRefGoogle Scholar
  75. Zeldis J, James MR, Grieve J, Richards L (2002) Omnivory by copepods in the New Zealand subtropical frontal zone. J Plankton Res 24:9–23CrossRefGoogle Scholar
  76. Zöllner E, Santer B, Boersma M, Hoppe HG, Jürgens K (2003) Cascading predation effects of Daphnia and copepods on microbial food web components. Freshw Biol 48:2174–219CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Dacha Atienza
    • 1
  • Albert Calbet
    • 1
  • Enric Saiz
    • 1
  • Miquel Alcaraz
    • 1
  • Isabel Trepat
    • 1
  1. 1.Institut de Ciències del Mar—CMIMA (CSIC)BarcelonaSpain

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