Skip to main content
Log in

Ontogenic changes of amino acid composition in planktonic crustacean species

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Changes in amino acid composition (AAC) during ontogeny of some planktonic crustacean species commonly found in fresh and brackish coastal waters were compared. For these comparisons two calanoid copepods (Eurytemora velox and Calanipeda aquae-dulcis), two cyclopoid copepods (Diacyclops bicuspidatus odessanus and Acanthocyclops robustus) and two Daphnia (Daphnia pulicaria and Daphnia magna) species were selected. A discriminant analysis was performed to determine whether there were significant differences between the AAC of the different stages of each species. Results show gradual changes in AAC during ontogeny of the copepod species. Calanoids showed the greatest differences in AAC between stages, followed by cyclopoids. Gradual changes in AAC were due to the increase in some amino acids such as alanine, valine, glutamic acid, glycine, arginine, proline and tyrosine from nauplii to adults. The latter showed a remarkable increase in all copepod species. In contrast, Daphnia species showed a relatively constant AAC during development, with only minor changes being detected, and not related with ontogeny. Differences in the physico-chemical variables of the lagoons do not seem to be the cause of copepod ontogenic changes in AAC. Data suggest that AAC differences found between stages of copepod species could indicate a gradual change in diet during the life cycle of these copepods.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aragão C, Conceição LEC, Dinis MT, Fyhn HJ (2004a) Amino acid pools of rotifers and Artemia under different conditions: nutritional implications for fish larvae. Aquaculture 234:429–445

    Article  Google Scholar 

  • Aragão C, Conceição LEC, Fyhn HJ, Dinis MT (2004b) Estimated amino acid requirements during early ontogeny in fish with different life styles: gilthead seabream (Sparus aurata) and Senegalese sole (Solea senegalesis). Aquaculture 242:589–605

    Article  Google Scholar 

  • Awapara J (1962) Free amino acids in invertebrates: a comparative study of the distribution and metabolism. In: Holden JT (ed) Amino acids pools. Elsevier Publishing Co., New York, pp 158–175

    Google Scholar 

  • Bechtel B (1995) Reptile and amphibian variants: colors, patterns, and scales. Krieger Publishing Co., Malabar, FL

    Google Scholar 

  • Becker C, Brepohl D, Feuchtmayr H, Zöllner E, Sommer F, Clemmesen C, Sommer U, Boersma M (2005) Impacts of copepods on marine seston, and resulting effects on Calanus finmarchicus RNA:DNA ratios in mesocosmos experiments. Mar Biol 146:531–541

    Article  CAS  Google Scholar 

  • Berggreen U, Hansen B, Kiørboe T (1988) Food size spectra, ingestion and growth of the copepod Acartia tonsa during development: implications for determination of copepod production. Mar Biol 99:341–352

    Article  Google Scholar 

  • Boersma M (1995) The allocation of resources to reproduction in Daphnia galeata: against the odds? Ecology 76:1251–1261

    Article  Google Scholar 

  • Bogdan KG, Gilbert JJ (1987) Quantitative comparison of food niches in some freshwater zooplankton. Oecology 72:331–340

    Article  CAS  Google Scholar 

  • Boix D, Gascón S, Sala J, Martinoy M, Gifre J, Quintana X (in press) Assessment of water quality in Mediterranean wetlands base don insect and crustacean assemblages: the case of Catalunya (NE Iberian Peninsula). Aquat Conserv: Mar Freshwat Ecosyst

  • Bonnet D, Carlotti F (2001) Development and egg production in Centropages typicus (Copepoda: Calanoida) fed different food types: a laboratory study. Mar Ecol Prog Ser 224:133–148

    Article  Google Scholar 

  • Brucet S, Quintana X, Boix D, López-Flores R, Badosa A, Moreno-Amich R (2005) Zooplankton structure and dynamics in permanent and temporary Mediterranean salt marshes: taxon-based and size-based approaches. Arch Hidrobiol 162:535–555

    Article  Google Scholar 

  • Burton RS (1991) Regulation of proline synthesis during osmotic stress in the copepod Tigriopus californicus. J Exp Zool 259:166–173

    Article  CAS  Google Scholar 

  • Carrillo P, Reche I, Cruz-Pizarro L (1996) Intraspecific stoichiometric variability and the ratio of nitrogen to phosporus resupplied by zooplankton. Freshwat Biol 36:363–374

    Article  CAS  Google Scholar 

  • Conceição LEC (1997) Growth in early life stages of fiches: an explanatory model. PhD thesis. Wageningen, The Netherlands: Wageningen Agricultural University, Wageningen, The Netherlands

  • Dabrowski K, Rusiecki M (1983) Content of total free amino acids in zooplanktonic food of fish larvae. Aquaculture 30:31–42

    Article  CAS  Google Scholar 

  • DeMott RW (1968) The role of taste in food selection by freshwater zooplankton. Oecologia 69:334–340

    Article  Google Scholar 

  • Deuchar EM (1962) The role of amino acid metabolism in developing encysted embryos of Artemia salina, the brine shrimp. Comp Biochem Physiol 20:245–261

    Google Scholar 

  • Forward R, Fyhn HJ (1983) Osmotic regulation of the krill, Maganyctiphanes novergica. Comp Biochem Physiol 74A:301–305

    Article  Google Scholar 

  • Fyhn HJ (1976) Holeuryhalinity and its mechanisms in a cirriped crustacean, Balanus improvisus. Comp Biochem Physiol 53A:19–30

    Article  CAS  Google Scholar 

  • Fyhn HJ, Finn RN, Helland S, Rønnestad I, Lømsland ER (1993) Nutritional value of phyto- and zooplankton as live food for marine fish larvae. In: Reinertsen H, Dahle LA, Jørgensen L, Tvinnereim K (eds) Fish Farming Technology. Balkema Publisher, Rotterdam, pp 121–126

    Google Scholar 

  • Gäde D, Grieshaber MK (1986) Pyruvate reductases catalyze the formation of lactate and opines in anaerobic invertebrates. Comp Biochem Physiol 83B:255–272

    Article  Google Scholar 

  • Gascón S, Boix D, Sala J, Quintana X (2005) Variability of benthic assemblages in relation to the hydrological pattern in Mediterranean salt marshes (Empordá wetlands, NE Iberian Peninsula). Arch Hydrobiol 163:163–181

    Article  Google Scholar 

  • Gophen M (1977) Food and feeding habits of Mesocyclops leuckarti (Claus) in lake Kinneret (Israel). Freshwat Biol 7:513–518

    Article  Google Scholar 

  • Guisande C, Maneiro I, Riveiro I (2000) Comparisons among the amino acid composition of females, eggs and food to determine the relative importance of food quantity and food quality to copepod reproduction. Mar Ecol Progr Ser 202:135–142

    Article  CAS  Google Scholar 

  • Guisande C, Maneiro I, Riveiro I, Barreiro A, Pazos Y (2002) Estimation of copepod trophic niche in the field using amino acids and marker pigments. Mar Ecol Prog Ser 239:147–156

    Article  CAS  Google Scholar 

  • Guisande C, Bartumeus F, Ventura M, Catalan J (2003) Role of food partitioning in structuring the zooplankton community in mountain lakes. Oecol 136:627–634

    Article  CAS  Google Scholar 

  • Hansen J, Bjørsen PK (1997) Zooplankton grazing and growth: scaling within the 2–2,000-μm body size range. Limnol Oceanogr 42:687–704

    Article  Google Scholar 

  • Hansen B, Bjørnsen PK, Hansen PJ (1994) The size ratio between planktonic predators and their prey. Limnol Oceanogr 39:395–403

    Article  Google Scholar 

  • Haond C, Bonnal L, Sandeaux R, Charmantier G, Trilles JP (1999) Ontogeny of intracellular isosmotic regulation in the European lobster Homarus gammarus (L.). Physiol Biochem Zool 72:534–544

    Article  CAS  Google Scholar 

  • Helland S, Triantaphyllidis GV, Fyhn HJ, Evjen MS, Lavens P, Sorgeloos P (2000) Modulation of the free amino acid pool and protein content in populations of the brine shrimp Artemia spp. Mar Biol 137:1005–1016

    Article  CAS  Google Scholar 

  • Helland S, Terjesen BF, Berg L (2003a) Free amino acids and protein content in the planktonic copepod Temora longicornis compared to Artemia franciscana. Aquaculture 215:213–228

    Article  CAS  Google Scholar 

  • Helland S, Nejstgaard JC, Fyhn HJ, Egge J, Båmstedt U (2003b) Effects of starvation, season, and diet on the free amino acid and protein content of Calanus finmarchicus females. Mar Biol 143:297–306

    Article  CAS  Google Scholar 

  • Huggins AK, Munday KA (1968) Crustacean metabolisms. In: Lowenstein O (ed) Advances in comparative physiology and biochemistry. Academic press, New York, pp 271–378

    Google Scholar 

  • Jamieson CD (1980) The predatory feeding of copepodid stages III to adults Mesocyclops leuckarti (Claus). In: Kerfoot WC (ed) Evolution and ecology of zooplankton communities. University Press of New England, Hanover (NH), London, pp 518–537

    Google Scholar 

  • Jin T, Qian PY (2004) Effect of amino acid on larval metamorphosis of the polychaete Hydroides elegans. Mar Ecol Prog Ser 267:209–218

    Article  CAS  Google Scholar 

  • Kimmel DG, Bradley BP (2001) Specific protein responses in the calanoid copepod Eurytemora affinis (Poppe, 1880) to salinity and temperature variation. J Exp Mar Biol Ecol 266:135–149

    Article  CAS  Google Scholar 

  • Laabir M, Poulet SA, Cueff A, Ianora A (1999) Effect of diet on levels of amino acids during embryonic and naupliar development of the copepod Calanus helgolandicus. Mar Biol 134:89–98

    Article  CAS  Google Scholar 

  • Legendre P, Legendre L (1998). Numerical ecology. Elsevier, Amsterdam, The Netherlands

    Google Scholar 

  • Maly EJ, Maly MP (1974) Dietary differences between two co-occurring calanoid copepod species. Oecology 17:325–333

    Article  Google Scholar 

  • Mente E, Houlihan DF, Smith K (2001) Growth, feeding frequency, protein turnover, and amino acid metabolism in European lobster Homarus gammarus L. J Exp Zool 289:419–432

    Article  CAS  Google Scholar 

  • Mullin MM, Brooks ER (1967) Laboratory culture, growth rate, and feeding behaviour of a planktonic marine copepod. Limnol Oceanogr 12:657–666

    Article  Google Scholar 

  • Ng WK, Hung SSO (1994) Amino acid composition of wholebody, egg and selected tissues of white sturgeon (Acipenser transmontanus). Aquaculture 126:329–339

    Article  CAS  Google Scholar 

  • Paffenhöfer GA (1971) Grazing and ingestion rates of nauplii, copepodids and adults of the marine planktonic copepod Calanus helgolandicus. Mar Biol 11:286–299

    Article  Google Scholar 

  • Poulet SA (1977) Grazing of marine copepod development stages on naturally occurring particles. J Fish Res Board Can 34:2381–2387

    Article  Google Scholar 

  • Régnault M (1971) Acides aminés libres chez les larves de Crangon septempinosa (Caridea) Variation de leur taux de l’éclosion à la mètamorphose Leur rôle au cours de développement et leur importance dans la nutrition. Mar Biol 11:35–44

    Article  Google Scholar 

  • Rosa R, Nunes ML (2003) Seasonal changes in nucleic acids, amino acids and protein content in juvenile Norway lobster (Nephrops novergicus). Mar Biol 143:565–572

    Article  CAS  Google Scholar 

  • Santer B, van den Bosch F (1994). Herbivorous nutrition of Cyclops vicinus: the effect of a pure algal diet on feeding, development, reproduction and life cycle. J Plankton Res 16:171–195

    Article  Google Scholar 

  • Schulz KL (1996) The nutrition of two cladocerans, the predaceous Bythotrephes cederstroemi and the herbivorous Daphnia pulicaria (nutrient recycling). PhD Thesis, University of Michigan, Michigan

  • Simpson JW, Alle K, Awapara J (1959) Free amino acids in some aquatic invertebrates. Biol Bull Mar Biol Lab, Woods Hole 117:371–381

    Article  CAS  Google Scholar 

  • Sterner RW (1993) Daphnia growth on varying quality of Scenedesmus: mineral limitation of zooplankton. Ecology 74:2352–2360

    Article  Google Scholar 

  • Swadling KM, Marcus NH (1994) Selectivity in the natural diets of Acartia tonsa Dana (Copepoda: Calanoida): Comparison of juveniles and adults. J Exp Mar Biol Ecol 181:91–103

    Article  Google Scholar 

  • Trobajo R, Quintana XD, Moreno-Amich R (2002) Model of alternative predominance of phytoplankton-periphyton-macrophytes in lentic waters of Mediterranean coastal wetlands. Arch Hydrobiol 154:19–40

    Article  CAS  Google Scholar 

  • Van Wandelen CH, Cohen SA (1997) Using quaternary high-performance liquid chromatography eluent systems for separating 6-aminoquinolyl-N-hydroxysuccinimidyl carbamate-derivated amino acid mixtures. J Chromatogr 763:11–22

    Article  CAS  Google Scholar 

  • Vilela MH (1992) Mass culture and nutritional quality of the marine copepod Tigriopus brevicornis Muller. Bol Inst Nac Pescas, Lisboa 17:49–63

    Google Scholar 

  • Wagner M, Durbin E, Buckley L (1998) RNA:DNA ratios as indicators of nutritional condition in the copepod Calanus finmarchicus. Mar Ecol Prog Ser 162:173–181

    Article  CAS  Google Scholar 

  • Wagner MM, Campbell RG, Boudreau CA, Durbin EG (2001) Nucleic acids and growth of Calanus finmarchicus in the laboratory under different food and temperature conditions. Mar Ecol Prog Ser 221:185–197

    Article  CAS  Google Scholar 

  • Zánkai PN (1991) Feeding of nauplius stages Eudiaptomus gracilis on mixed plastic beads. J Plankton Res 13:437–453

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant from the Comisión de Investigación Científica y Técnica (CICYT), Programa Nacional de Biodiversidad, Ciencias de la Tierra y Cambio Global (ref. CGL 2004-05433/BOS) and by a FI grant of Comissionat per a Universitats i Recerca de la Generalitat de Catalunya. We sincerely thank Cástor Guisande for help in amino acid analysis and the revision of an earlier version of the paper and E. Shubert and Lara Arroyo for revising the English.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sandra Brucet.

Additional information

Communicated by S.A. Poulet, Roscoff

Rights and permissions

Reprints and permissions

About this article

Cite this article

Brucet, S., Boix, D., López-Flores, R. et al. Ontogenic changes of amino acid composition in planktonic crustacean species. Marine Biology 148, 131–139 (2005). https://doi.org/10.1007/s00227-005-0068-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-005-0068-4

Keywords

Navigation