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.
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
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
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
Bechtel B (1995) Reptile and amphibian variants: colors, patterns, and scales. Krieger Publishing Co., Malabar, FL
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
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
Boersma M (1995) The allocation of resources to reproduction in Daphnia galeata: against the odds? Ecology 76:1251–1261
Bogdan KG, Gilbert JJ (1987) Quantitative comparison of food niches in some freshwater zooplankton. Oecology 72:331–340
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
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
Burton RS (1991) Regulation of proline synthesis during osmotic stress in the copepod Tigriopus californicus. J Exp Zool 259:166–173
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
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
DeMott RW (1968) The role of taste in food selection by freshwater zooplankton. Oecologia 69:334–340
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
Forward R, Fyhn HJ (1983) Osmotic regulation of the krill, Maganyctiphanes novergica. Comp Biochem Physiol 74A:301–305
Fyhn HJ (1976) Holeuryhalinity and its mechanisms in a cirriped crustacean, Balanus improvisus. Comp Biochem Physiol 53A:19–30
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
Gäde D, Grieshaber MK (1986) Pyruvate reductases catalyze the formation of lactate and opines in anaerobic invertebrates. Comp Biochem Physiol 83B:255–272
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
Gophen M (1977) Food and feeding habits of Mesocyclops leuckarti (Claus) in lake Kinneret (Israel). Freshwat Biol 7:513–518
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
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
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
Hansen J, Bjørsen PK (1997) Zooplankton grazing and growth: scaling within the 2–2,000-μm body size range. Limnol Oceanogr 42:687–704
Hansen B, Bjørnsen PK, Hansen PJ (1994) The size ratio between planktonic predators and their prey. Limnol Oceanogr 39:395–403
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
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
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
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
Huggins AK, Munday KA (1968) Crustacean metabolisms. In: Lowenstein O (ed) Advances in comparative physiology and biochemistry. Academic press, New York, pp 271–378
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
Jin T, Qian PY (2004) Effect of amino acid on larval metamorphosis of the polychaete Hydroides elegans. Mar Ecol Prog Ser 267:209–218
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
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
Legendre P, Legendre L (1998). Numerical ecology. Elsevier, Amsterdam, The Netherlands
Maly EJ, Maly MP (1974) Dietary differences between two co-occurring calanoid copepod species. Oecology 17:325–333
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
Mullin MM, Brooks ER (1967) Laboratory culture, growth rate, and feeding behaviour of a planktonic marine copepod. Limnol Oceanogr 12:657–666
Ng WK, Hung SSO (1994) Amino acid composition of wholebody, egg and selected tissues of white sturgeon (Acipenser transmontanus). Aquaculture 126:329–339
Paffenhöfer GA (1971) Grazing and ingestion rates of nauplii, copepodids and adults of the marine planktonic copepod Calanus helgolandicus. Mar Biol 11:286–299
Poulet SA (1977) Grazing of marine copepod development stages on naturally occurring particles. J Fish Res Board Can 34:2381–2387
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
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
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
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
Sterner RW (1993) Daphnia growth on varying quality of Scenedesmus: mineral limitation of zooplankton. Ecology 74:2352–2360
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
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
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
Vilela MH (1992) Mass culture and nutritional quality of the marine copepod Tigriopus brevicornis Muller. Bol Inst Nac Pescas, Lisboa 17:49–63
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
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
Zánkai PN (1991) Feeding of nauplius stages Eudiaptomus gracilis on mixed plastic beads. J Plankton Res 13:437–453
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
Corresponding author
Additional information
Communicated by S.A. Poulet, Roscoff
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-005-0068-4