Abstract
Grass shrimp, Palaemonetes pugio, were capable of hypo- and hyper-osmotic regulation of body fluids. Hemolymph chloride and osmotic concentrations were maintained at relatively stable levels over a wide salinity range. Following an abrupt transfer from intermediate (14 and 17‰) to high (31 and 35‰) or low (1 and 2‰) salinities, hemolymph chloride levels exhibited initial overshoot and undershoot, respectively, of new steady-state levels. Osmotic concentrations exhibited an initial undershoot at low, but not overshoot at high salinity. Chloride space in salinity-acclimated shrimp was relatively stable at salinities from 1 to 35‰. Changes in chloride space following salinity transfer paralleled those of hemolymph chloride levels, and are discussed in the light of alterations in intracellular sodium concentrations reported earlier. Rate constants for chloride turnover indicated independent exchanges of sodium and chloride ions. Water-turnover measurements showed that permeability of P. pugio was greatest at the isosmotic salinity (17‰) and reduced at salinities which were associated with active osmoregulation. Exposure to sublethal and 96-h LC50 levels of Aroclor® 1254 did not seriously alter hemolymph chloride and osmotic concentrations, chloride space or chloride-exchange kinetics in adult shrimp. Disruption of hemolymph chloride regulation in juvenile shrimp was associated with large mortalities not observed in adults. Shrimp exposed to Aroclor 1254 at 17‰ S exhibited reduced water permeability similar to levels previously observed in controls at high and low salinities in response to osmotic or ionic gradients. Exposure to PCBs did not result in further reduction in permeability at the latter salinities.
Similar content being viewed by others
Literature Cited
Capen, R.L.: Studies of water uptake in the euryhaline crab, Rithropanopeus harrisii. J. exp. Zool. 182, 307–319 (1972)
Comar, C.L.: Radioisotopes in biology and agriculture, 481 pp. New York: McGraw-Hill Book Co., Inc. 1955
Crump-Weisner, H.J., H.R. Feltz and M.L. Yates: A study of the distribution of polychlorinated biphenyls in the aquatic environment. Pestic. Monit. J. 8, 157–161 (1974)
Cutkomp, L.K., H.H. Yap, E.Y. Cheng and R.B. Koch: ATPase activity in fish tissue homogenates and inhibitory effects of DDT and related compounds. Chem. biol. Interactions 3, 439–447 (1971)
—, D. Desaiah and R.B. Koch: The sensitivity of fish ATPase to polychlorinated biphenyls. Envir. Hlth Perspectives exp. Iss. 1, 165–168 (1972)
Dehnel, P.A.: Aspects of osmoregulation in two species of intertidal crabs. Biol. Bull. mar. biol. Lab., Woods Hole 122, 208–227 (1962)
Desaiah, D., L.K. Cutkomp, R.B. Koch and A. Jarvinen: DDT: effect of continuous exposure on ATPase activity in fish, Pimephales promelas. Archs envir. Contam. Toxicol. 3, 132–141 (1975)
— H.H. Yap and R.B. Koch: Inhibition of oligomycin-sensitive and insensitive Mg++-ATPase in fish by polychlorinated biphenyls. Biochem. Pharmac. 21, 857–865 (1972)
Dobkins, S. and R.B. Manning: Osmoregulation in two species of Palaemonetes (Crustacea: Decapoda) from Florida. Bull. mar. Sci. Gulf Caribb. 14, 149–157 (1964)
Duke, T.W., J.I. Lowe and A.J. Wilson, Jr.: A polychlorinated biphenyl (Aroclor 1254) in the water, sediment, and biota of Escambia Bay, Florida. Bull. envir. Contam. Toxicol. 5, 171–180 (1970)
Eisler, R. and P. Edmunds: Effects of endrin on blood and tissue chemistry of a marine fish. Trans. Am. Fish. Soc. 95, 153–159 (1966)
Giam, C.S., A.R. Hanks, R.L. Richardson, W.M. Sackett and M.K. Wong: DDT, DDE, and PCBs in biota from the Gulf of Mexico and Caribbean Sea 1971. Pestic. Monit. J. 6, 139–159 (1972)
Grant, B.F. and P.M. Merle: Chronic endrin poisoning in goldfish Carassius auratus. J. Fish. Res. Bd Can. 27, 2225–2232 (1970)
Green, M.B.: Polychloroaromatics and heteroaromatics of industrial importance. In: Polychloroaromatic compounds, pp 403–474. Ed. by H. Suchitsky. New York: Plenum Press 1974
Gross, W.H.: An analysis of response to osmotic stress in selected decapod Crustacea. Biol. Bull. mar. biol. Lab., Woods Hole 122, 43–62 (1957)
Hagerman, L.: Osmoregulation and sodium balance in Crangon vulgaris (Fabricius) (Crustacea, Natantia) in varying salinities. Ophelia 9, 21–30 (1971)
Hansen, D.J., P.R. Parrish and J. Forester: Aroclor 1016: toxicity to and uptake by estuarine animals. Envir. Res. 7, 363–373 (1974a)
— J.I. Lowe, A.J. Wilson, Jr. and P.D. Wilson: Chronic toxicity, uptake and retention of Aroclor 1254 in two estuarine fishes. Bull. envir. Contam. Toxicol. 6, 113–119 (1971)
Hansen, D.J., S.C. Schimmel and E. Matthews: Avoidance of Aroclor 1254 by shrimp and fishes. Bull. envir. Contam. Toxicol. 12, 253–256 (1974b)
Holthuis, L.B.: A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas II. Subfamily Palaemoniae. Occ. Pap. Allan Hancock Fdn 12, 1–369 (1952)
Jampol, L.M. and F.H. Epstein: Na+−K+ activated ATPase and osmotic regulation by fishes. Am. J. Physiol. 218, 607–611 (1970)
Janicki, R.H. and W.B. Kinter: DDT: disrupted osmoregulatory events in the intestine of the eel Anguilla rostrata adapted to seawater. Science, N.Y. 173, 1146–1148 (1971a)
—: DDT inhibits Na+, K+, Mg++-ATPase in intestinal mucosa and gills of marine teleosts. Nature, Lond. 233, 148–149 (1971b)
Kinne, O.: Physiology of estuarine organisms with special reference to salinity and temperature. In: Estuaries, pp 525–540. Ed. by G.H. Lauff, Washington, D.C.: American Association for the Advancement of Science 1967 (Publs Am. Ass. Advmt Sci. No. 83)
—: Salinity: animals—invertebrates. In: Marine ecology. Vol. I. Environmental factors, Part 2. pp 821–995. Ed. by O. Kinne. London: Wiley-Interscience 1971
Kinter, W.B., L.S. Merkens, R.H. Janicki and A.M. Guarino: Studies on the mechanisms of DDT and polychlorinated biphenyls: disruption of osmoregulation in marine fish. Envir. Hlth Perspectives exp. Iss. 1, 169–173 (1972)
Kirschner, L.B.: The study of NaCl transport in aquatic animals. Am. Zool. 10, 165–376 (1970)
Koch, R.B., L.K. Cutkomp and H.H. Yap: Inhibition of oligomycin sensitive and insensitive fish ATPase activity by chlorinated hydrocarbon insecticides. Biochem. Pharmac. 20, 3243–3245 (1971)
—, D. Desaiah, H.H. Yap and L.K. Cutkomp: Polychlorinated biphenyls: effects of long-term exposure on ATPase activity in fish, Pimephales promelas. Bull. envir. Contam. Toxicol. 7, 87–92 (1972)
Lockwood, A.P.M.: Aspects of the physiology of Crustacea, 328 pp. San Francisco: W.H. Freeman & Co. 1967
—, C.B.E. Inman and T.H. Courtenay: The influence of environmental salinity on the water fluxes of the amphipod crustacean Gammarus duebeni. J. exp. Biol. 58, 137–148 (1973)
Lucu, Č., G. Roesijadi and J.W. Anderson: Sodium kinetics in the shrimp Palaemonetes pugio I. Steady-state and nonsteady-state experiments. J. comp. Physiol. (In press). (1976)
—, D. Siebers and K.R. Sperling: Comparison of osmoregulation between Adriatic and North Sea Carcinus. Mar. Biol. 22, 85–95 (1973)
Lynch, M.P. and K.W. Webb: Variations in serum constituents of the blue crab, Callinectes sapidus: free amino acids and total ninhydrin positive substances. Comp. Biochem. Physiol. 45B, 407–418 (1973)
—— and W.A. van Engel: Variations in serum constituents of the blue crab Callinectes sapidus: chloride and osmotic concentrations. Comp. Biochem. Physiol. 44A, 719–734 (1973)
Maetz, J.: Aspects of adaptation to hypo-osmotic and hyper-osmotic environments. In: Biochemical and biophysical perspectives in marine biology, pp 1–167. Ed. by D.C. Malins and J.R. Sargent. New York: Academic Press 1974
Nimmo, D.R. and L.H. Bahner: Some physiological consequences of polychlorinated biphenyl-and salinity-stress in penaeid shrimp. In: Pollution and physiology of marine organisms, pp 427–443. Ed. by F.J. Vernberg and W.B. Vernberg. New York, San Francisco: Academic Press 1974
—, R.R. Blackman, A.J. Wilson, Jr. and J. Forester: Toxicity and distribution of Aroclor® 1254 in the pink shrimp Penaeus duoarum. Mar. Biol. 11, 191–197 (1971)
—, J. Forester, P.T. Heitmuller and G.H. Cook: Accumulation of Aroclor 1254 in grass shrimp (Palaemonetes pugio) in laboratory and field exposures. Bull. envir. Contam. Toxicol. 11, 303–308 (1974)
—, D.J. Hansen, J.A. Couch, N.R. Cooley, P.R. Parrish and J.I. Lowe: Toxicity of Aroclor 1254 and its physiological activity in several estuarine organisms. Archs envir. Contam. Toxicol. 3, 22–39 (1975)
Nisbet, I.C.T. and A.F. Sarofim: Rates and routes of transport of PCBs in the environment. Envir. Hlth Perspectives exp. Iss. 1, 21–38 (1972)
Nixon, S.W. and C.A. Oviatt: Ecology of a New England salt marsh. Ecol. Monogr. 43, 463–498 (1973)
Panikkar, N.K.: Osmotic behavior of Palaemonetes varians (Leach). Nature, Lond. 144, 866–867 (1939)
Peakall, D.B.: Polychlorinated biphenyls: occurrence and biological effects. Residue Rev. 44, 1–21 (1972)
Pfeiler, E. and L.B. Kirschner: Studies on gill ATPase of rainbow trout. Biochim. biophys. Acta 282, 301–310 (1972)
Potts, W.T.W. and G. Parry: Sodium and chloride balance in the prawn, Palaemonetes varians. J. exp. Biol. 41, 591–601 (1964a)
——: Osmotic and ionic regulation in animals, 423 pp. Oxford: Pergamon Press 1964b
Renfro, J.L., B. Schmidt-Nielsen, D. Miller, D. Benos and J. Allen: Methyl mercury and inorganic mercury; uptake, distribution, and effect on osmoregulatory mechanisms in fishes. In: Pollution and physiology of marine organisms, pp 101–122. Ed. by F.J. Vernberg and W.B. Vernberg. New York, San Francisco: Academic Press 1974
Riggs, D.S.: The mathematical approach to physiological problems, 445 pp. Cambridge, Massachusetts: The M.I.T. Press 1963
Risebrough, R.W. and B. DeLappe: Accumulation of polychlorinated biphenyls in ecosystems. Envir. Hlth Perspectives exp. Iss. 1, 39–45 (1972)
——, P. Rieche, S.G. Herman, D.B. Peakall and M.N. Kowen: Polychlorinated biphenyls in the global ecosystem. Nature, Lond. 220, 1098–1102 (1968)
Roesijadi, G., S.R. Petrocelli, J.W. Anderson, C.S. Giam and G.E. Neff. Toxicity of polychlorinated biphenyls (Aroclor 1254) to adult, juvenile and larval stages of the shrimp Palaemonetes pugio. Bull. envir. Contam. Toxicol. 15, 297–304 (1976)
Rudy, P.P.: Water permeability in selected decapod Crustacea. Comp. Biochem. Physiol. 22, 581–589 (1967)
Schmidt-Nielsen, B.: Osmoregulation: effect of salinity and heavy metals. Fedn Proc. Fedn Am. Socs exp. Biol. 33, 2137–2146 (1974)
Siebers, D., Č. Lucu, K.R. Sperling and K. Eberlein: Kinetics of osmoregulation in the crab Carcinus maenas. Mar. Biol. 17, 291–303 (1972)
Smith, R.: Osmotic regulation and adaptive reduction of water permeability in a brackishwater crab, Rithropanopeus harrisi (Brachyura, Xanthidae). Biol. Bull. mar. biol. Lab., Woods Hole 133, 643–658 (1967)
—: The apparent water-permeability of Carcinus maenas (Crustacea, Brachyura, Portunidae) as a function of salinity. Biol. Bull. mar. biol. Lab., Woods Hole 138, 351–362 (1970)
— and P.P. Rudy: Water exchange in the crab Hemigrapsus nudus measured by use of deuterium and tritium oxides as tracers. Biol. Bull. mar. biol. Lab., Woods Hole 143, 234–246 (1972)
Sokal, R.R. and F.J. Rohlf: Biometry, 776 pp. San Francisco: W.H. Freeman & Co. 1969
Spaargaren, D.H.: Determination of the extracellular volume in the shrimp Crangon crangon (L.). Comp. Biochem. Physiol. 43A, 843–849 (1972)
Thompson, L.C. and A.W. Pritchard: Osmoregulatory capacities of Callianassa and Upogebia (Crustacea: Thalassinidea). Biol. Bull. mar. Biol. Lab., Woods Hole 136, 114–129 (1969)
Thorp, J.H. and D.E. Hoss: Effects of salinity and cyclic temperature on survival of grass shrimp (Palaemonetes), and their relationship to natural distributions. J. exp. mar. Biol. Ecol. 18, 19–28 (1975)
Weber, R.E. and W.J.A. van Marrewijk: Free amino acids and isosmotic intracellular regulation in the shrimp Crangon crangon. Life Sciences 11, 589–595 (1972)
Welsh, B.L.: The role of grass shrimp, Palaemonetes pugio, in a tidal marsh ecosystem. Ecology 56, 513–530 (1975)
Wood, C.E.: Physioecology of the grass shrimp, Palaemonetes pugio, in the Galveston Bay estuarine system. Contr. mar. Sci. Univ. Texas 12, 54–79 (1967)
Yap, H.H., D. Desaiah and L.K. Cutkomp: Sensitivity of fish ATPases to polychlorinated biphenyls. Nature, Lond. 232, 61–62 (1971)
Zitko, V. and P.M. K. Choi: PCB and other industrial halogenated hydrocarbons in the environment. Tech. Rep. Fish. Res. Bd Can. 272, 1–64 (1971)
Author information
Authors and Affiliations
Additional information
Communicated by M.R. Tripp, Newark
Rights and permissions
About this article
Cite this article
Roesljadi, G., Anderson, J.W., Petrocelli, S.R. et al. Osmoregulation of the grass shrimp Palaemonetes pugio exposed to polychlorinated biphenyls (PCBs). I. Effecton chloride and osmotic concentrations and chloride-and water-exchange kinetics. Mar. Biol. 38, 343–355 (1976). https://doi.org/10.1007/BF00391374
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00391374