Skip to main content

Biochemical responses during starvation and subsequent recovery in postlarval Pacific white shrimp, Penaeus vannamei

Abstract

Postlarval shrimp, Penaeus vannamei Boone, 1931, were held individually in cages and exposed to two feeding regimes. One group was starved for 12 d and then fed during the following 12 d. A second group was fed throughout the 24 d study. Four individuals were sampled from each of the two groups on Days 0, 1, 2, 4, 8, 12, 13, 14, 16, 20, and 24. Molting and growth among the starved-fed postlarvae stopped after 2 d starvation, while fed postlarvae increased significantly in size throughout the 24 d study. Among the starved-fed postlarvae, water content increased rapidly in response to starvation. DNA and sterol concentrations increased significantly during starvation due to selective catabolism of cellular components. After 12 d, RNA concentration was not significantly different between the fed and starved-fed postlarvae, but became significantly higher in the starved-fed postlarvae 48 h after feeding resumed. Triacylglycerol reserves were severely depleted during the first day of starvation, while protein concentrations began to decrease after the second day of starvation. RNA, protein, and the polyamines spermidine and spermine, when expressed as a ratio to DNA, decreased in response to starvation. Concentrations of all measured parameters in the starved-fed postlarvae returned to levels similar to those in the fed group 8 to 12 d after feeding resumed. Results of this study suggest that triacylglycerol provides energy during short periods of starvation, while protein is utilized during prolonged starvation. The ratios of RNA:DNA, protein:DNA, spermidine:DNA, spermine:DNA, two unidentified amine compounds, and percent water content are all useful indicators of prolonged nutritional stress in postlarval P. vannamei.

This is a preview of subscription content, access via your institution.

References

  1. Alikan MA (1972) Changes in the hepatopancreas metabolic reserves of Porcellio laevis Latrielle during starvation and the moult-cycle. Am Midl Nat 87: 503–513

    Google Scholar 

  2. Anger K (1984) Influence of starvation on moult cycle and morphogenesis of Hyas araneus larvae (Decapoda: Majidae). Helgoländer Meeresunters 38: 21–33

    Google Scholar 

  3. Anger K, Dawirs RR (1981) Influence of starvation on the larval development of Hyas araneus (Decapoda: Majidae). Helgoländer Meeresunters 34: 287–311

    Google Scholar 

  4. Anger K, Harms J, Püschel C, Seeger B (1989) Physiological and biochemical changes during the larval development of a brachyuran crab reared under constant conditions in the laboratory. Helgoländer Meeresunters 43: 225–244

    Google Scholar 

  5. Anger K, Hirche H-J (1990) Nucleic acids and growth of larval and early juvenile spider crab, Hyas araneus. Mar Biol 105: 403–411

    Google Scholar 

  6. Anger K, Storch V, Anger V, Capuzzo JM (1985) Effects of starvation on the moult cycle and hepatopancreas of stage I lobster (Homarus americanus) larvae. Helgoländer Meeresunters 39: 107–116

    Google Scholar 

  7. Barclay MC, Dall W, Smith DM (1983) Changes in lipid and protein during starvation and the moulting cycle in the tiger prawn, Penaeus esculentus (Haswell). Lexp mar Biol Ecol 68: 229–244

    Google Scholar 

  8. Barron MG, Adelman IR (1984) Nucleic acid, protein content, and growth of larval fish sublethally exposed to various toxicants. Can J Fish aquat Sciences 41: 141–150

    Google Scholar 

  9. Bligh EG, Dyer W (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911–917

    Google Scholar 

  10. Bourdier GG, Amblard CA (1989) Lipids in Acanthodiaptomus denticornis during starvation and fed on three different algae. J Plankton Res 11: 1201–1212

    Google Scholar 

  11. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Analyt Biochem 72: 248–254

    Google Scholar 

  12. Buckley LJ (1984) RNA-DNA ratio: an index of larval fish growth in the sea. Mar Biol 80: 291–298

    Google Scholar 

  13. Burton K (1956) A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribose nucleic acid. biochem J 62: 315–323

    Google Scholar 

  14. Chandumpai A, Dall W, Smith DM (1991) Lipid-class composition of organs and tissues of the tiger prawn Panaeus (sic) esculentus during the moulting cycle and during starvation. Mar Biol 108: 235–245

    Google Scholar 

  15. Clemmesen C (1994) The effect of food availability, age or size on the RNA/DNA ratio of individually measured herring larvae: laboratory calibration. Mar Biol 118: 377–382

    Google Scholar 

  16. Clemmesen CM (1987) Laboratory studies on RNA/DNA ratios of starved and fed herring (Clupea harengus) and turbot (Scophthalmus maximus) larvae. J Cons int Explor Mer 43: 122–128

    Google Scholar 

  17. Conover RJ (1964) Food relations and nutrition of zooplankton. Occ Publs Narragansett mar Lab, Univ Rhode Isl 2: 81–91 (Proc Symp exp mar Ecol)

    Google Scholar 

  18. Corti A, Tartoni PL, Astancolle S, Davalli P, Viviani R (1988) Liver ornithine decarboxylase activity in the European sea bass (Dicentrarchus labrax): effects of protein composition of the diet, environmental conditions and age. Comp Biochem Physiol 89B: 137–141

    Google Scholar 

  19. Cuzon G, Cahu C, Aldrin JF, Messager JL, Stephan G, Mevel M (1980) Starvation effect on metabolism of Penaeus japonicus. Proc Wld Maricult Soc 11: 410–423

    Google Scholar 

  20. Dagg MJ, Littlepage JL (1972) Relationships between growth rate and RNA, DNA, protein and dry weight in Artemia salina and Euchaeta elongata. Mar Biol 17: 162–170

    Google Scholar 

  21. Dall W (1974) Indices of nutritional state in the western rock lobster, Panulirus longipes (Milne Edwards). I. Blood and tissue constituents and water content. J exp mar Biol Ecol 16: 176–180

    Google Scholar 

  22. Dall W (1975) Indices of nutritional state in the western rock lobster, Panulirus longipes (Milne Edwards). II. Gastric fluid constituents. J exp mar Biol Ecol 18: 1–18

    Google Scholar 

  23. Davalli P, Carpene E, Serrazanetti GP, Bettuzzi S, Viviani R, Corti A (1990) Responses of polyamine metabolism to metal treatment (Co, Cu, Zn, Cd) in the liver of the goldfish (Carassius auratus): distinct effect of season and temperature. Comp Biochem Physiol 96C: 305–310

    Google Scholar 

  24. Dawirs RR (1987) Influence of limited starvation periods on growth and elemental composition (C,N,H) of Carcinus maenas (Decapoda: Portunidae) larvae reared in the laboratory. Mar Biol 93: 543–549

    Google Scholar 

  25. Fraser AJ (1989) Triacylglycerol content as a condition index for fish, bivalve, and crustacean larvae. Can J Fish aquat Sciences 46: 1868–1873

    Google Scholar 

  26. Hassett RP, Landry MR (1988) Short-term changes in feeding and digestion by the copepod Calanus pacificus. Mar Biol 99: 63–74

    Google Scholar 

  27. Hassett RP, Landry MR (1990) Effects of diet and starvation on digestive enzyme activity and feeding behavior of the marine copepod Calanus pacificus. J Plankton Res 12: 991–1010

    Google Scholar 

  28. Hazlett B, Rubenstein D, Rittschof D (1975) Starvation, energy reserves, and aggression in the crayfish Orconectes virilis (Hagen, 1870) (Decapoda, Cambaridae). Crustaceana 28: 11–16

    Google Scholar 

  29. Heath JR, Barnes H (1970) Some changes in biochemical composition with season and during the moulting cycle of the common shore crab, Carcinus maenas (L.). J exp mar Biol Ecol 5: 199–233

    Google Scholar 

  30. Heby O (1981) Role of polyamines in the control of cell proliferation and differentiation. Differentiation 19: 1–20

    Google Scholar 

  31. Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 52: 187–211

    Google Scholar 

  32. Juinio MAR, Cobb JS, Bengtson D, Johnson M (1992) Changes in nucleic acids over the molt cycle in relation to food availability and temperature in Homarus americanus postlarvae. Mar Biol 114: 1–10

    Google Scholar 

  33. Jungreis AM (1968) The role of stored glycogen during long-term temperature acclimation in the freshwater crayfish, Orconectes virilis. Comp Biochem Physiol 24: 1–6

    Google Scholar 

  34. Lehninger AL (1975) Biochemistry. 2nd edn. Worth Publishers Inc., New York

    Google Scholar 

  35. Lovett DL, Watts SA (1995). Changes in polyamine levels in response to acclimation to salinity in gills of the blue crab Callinectes sapidus Rathbun. Comp Biochem Physiol 10B: 115–119

    Google Scholar 

  36. Lovrich GA, Ouellet P (1994) Patterns of growth and triacylglycerol content in snow crab Chionoecetes opilio (Brachyura: Majidae) zoeal stages reared in the laboratory. Mar Biol 120: 585–591

    Google Scholar 

  37. Malloy KD, Targett TE (1994) The use of RNA:DNA ratios to predict growth limitation of juvenile summer flounder (Paralichthys dentatus) from Delaware and North Carolina estuaries. Mar Biol 118: 367–375

    Google Scholar 

  38. Moss SM (1994a) Use of nucleic acids as indicators of growth in juvenile white shrimp, Penaeus vannamei. Mar Biol 120: 359–367

    Google Scholar 

  39. Moss SM (1994b) Growth rates, nucleic acid concentrations, and RNA/DNA ratios of juvenile white shrimp, Penaeus vannamei Boone, fed different algal diets. J exp mar Biol Ecol 182: 193–204

    Google Scholar 

  40. Munro HN, Fleck A (1966) Recent developments in the measurement of nucleic acids in biological materials. Analyst, Lond 91: 78–88

    Google Scholar 

  41. Nes WR (1974) Role of steroids in membranes. Lipids 9: 596–612

    Google Scholar 

  42. Ogle JT, Beaugez K, Lotz JM (1992) Effects of salinity on survival and growth of postlarval Penaeus vannamei. Gulf Res Rep 8: 415–421

    Google Scholar 

  43. Ota AY, Landry MR (1984) Nucleic acids as growth rate indicators for early developmental stages of Calanus pacificus Brodsky. J exp mar Biol Ecol 80: 147–160

    Google Scholar 

  44. Ouellet P, Taggart CT, Frank KT (1992) Lipid condition and survival in shrimp (Pandalus brealis) larvae. Can J Fish aquat Sciences 49: 368–378

    Google Scholar 

  45. Pegg AE (1988) Polyamine metabolism and its importance in neoplastic growth and as a target for chemotherpy. Cancer Res 48: 759–774

    Google Scholar 

  46. Regnault M (1981) Respiration and ammonia excretion of the shrimp Crangon crangon L.: Metabolic response to prolonged starvation. J comp Physiol 141: 549–555

    Google Scholar 

  47. Regnault M, Luquet P (1974) Study by evolution of nucleic acid content of prepuberal growth in the shrimp Crangon vulgaris. Mar Biol 25: 291–298

    Google Scholar 

  48. Sasaki GC (1984) Biochemical changes associated with embryonic and larval development in the American lobster Homarus americanus Milne Edwards. Ph.D. thesis. Massachusetts Institute of Technology, Woods Hole Oceanographic Institution (Ref. 84-8)

  49. Sasaki GC, Capuzzo JM, Biesiot P (1986) Nutritional and bioenergetic considerations in the development of the American lobster Homarus americanus. Can J Fish aquat Sciences 43: 2311–2319

    Google Scholar 

  50. Schafer HJ (1968) Storage materials utilized by starved pink shrimp, Penaeus duorarum Burkenroad. FAO Fish Rep 57: 393–403

    Google Scholar 

  51. Speck U, Urich K (1969) Consumption of body constituents during starvation in the crayfish, Orconectes limosus. Z vergl Physiol 63: 410–414

    Google Scholar 

  52. Steeves HR (1963) The effects of starvation on glycogen and lipid metabolism in the isopod Linceus brachyurus (Harger). J exp Zool 154: 21–38

    Google Scholar 

  53. Stuck KC, Overstreet RM (1994) Effect of Baculovirus penaei on growth and survival of experimentally infected postlarvae of the Pacific white shrimp, Penaeus vannamei. J Invert Path 24: 18–25

    Google Scholar 

  54. Tabor CW, Tabor H (1984) Polyamines. A Rev Biochem 53: 749–790

    Google Scholar 

  55. Virtue P, Nicol S, Nichols PD (1993) Changes in the digestive gland of Euphausia superba during short-term starvation: lipid class, fatty acid and sterol content and composition. Mar Biol 117: 441–448

    Google Scholar 

  56. Vogt G, Storch V, Quinito ET, Pascual FP (1985) Midgut gland as monitor organ for the nutritional value of diets in Penaeus monodon (Decapoda). Aquaculture, Amsterdam 48: 1–12

    Google Scholar 

  57. Wallace JC, (1993) Feeding, starvation and metabolic rate in the shore crab Carcinus maenas. Mar Biol 20: 277–281

    Google Scholar 

  58. Wang SY, Lum JL, Carls MG, Rice SD (1993) Relationship between growth and total nucleic acids in juvenile pink salmon, Oncorhynchus gorbuscha, fed crude oil contaminated food. Can J Fish aquat Sciences 50: 996–1001

    Google Scholar 

  59. Wang SY, Stickle, WB (1986) Changes in nucleic acid concentration with starvation in the blue crab Callinectes sapidus Rathbun. J Crustacean Biol 6: 49–56

    Google Scholar 

  60. Watts SA, Lee KJ, Cline GB (1994) Elevated ornithine decarboxylase activity and polyamine levels during early development in the brine shrimp Artemia franciscana. J exp Zool 270: 426–431

    Google Scholar 

  61. Watts SA, Wang, SY, Castille, FL, Lawrence, AL (1992) Biochemical evaluation of shrimp growth: polyamine analysis. Abstracts. Aquaculture '92, May 21–25, 1992. World Aquaculture Society, Baton Rouge, La, USA (Unpublished program abstract)

    Google Scholar 

  62. Watts SA, Yeh EW, Henry R (1996) Hypoosmotic stimulation of ornithine decarboxylase activity in the brine shrimp Artemia franciscana. J exp zool (In press)

  63. Wilcox JR, Jeffries HP (1976) Hydration in the sand shrimp Crangon septemspinosa: relation to diet. Biol Bull mar biol Lab, Woods Hole 150: 522–530

    Google Scholar 

  64. Wyban JA, Swingle JS, Sweeny JN, Pruder GD (1992) Development and commercial performance of high health shrimp using specific pathogen free (SPF) broodstock Penaeus vannamei. In: Wyban JA (ed) Proceedings of the Special Session on Shrimp Farming. World Aquaculture Society, Baton Rouge, Louisiana, pp 254–260

    Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to K. C. Stuck.

Additional information

Communicated by N.H. Marcus, Tallahassee

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Stuck, K.C., Watts, S.A. & Wang, S.Y. Biochemical responses during starvation and subsequent recovery in postlarval Pacific white shrimp, Penaeus vannamei . Marine Biology 125, 33–45 (1996). https://doi.org/10.1007/BF00350758

Download citation

Keywords

  • Cage
  • Triacylglycerol
  • Spermine
  • Spermidine
  • Biochemical Response