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Opioid systems, behavioral thermoregulation and shell polymorphism in the land snail, Cepaea nemoralis

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Summary

Numerous ecological studies have dealt with the shell color and banding polymorphism of the land snail Cepaea nemoralis. The present field and laboratory investigations focus on the roles of opioid systems in modulating the thermal preferences and behavioral thermoregulation of various morphological types of Cepaea. Evidence is presented that differences in opioid modulation of the thermal responses of Cepaea are associated with shell polymorphism. It is shown that the effects of the prototypic opiate agonist, morphine, and antagonist, naloxone, on behavioral thermoregulation in Cepaea vary with the shell banding pattern and thermal microhabitat. In both the field and laboratory, morphine (0.10, 1.0 and 10 μg per snail) caused significant dose- and time-dependent increases in the temperatures selected by various morphological types of Cepaea. The palest shell type (yellow, unbanded) with the highest basal preferred temperature displayed the greatest response to morphine, the shell type (yellow, 2-banded) with an intermediate basal preferred temperature showed an intermediate response to morphine, and the darkest shell type (yellow, 5-banded) with lowest basal preferred temperature showed the least increase in preferred temperature after administration of morphine. These effects of morphine were blocked and reversed by naloxone (1.0 μg), with the opiate antagonist by itself (1.0 and 10 μg) causing a significant decrease in behaviorally selected temperatures. The unbanded and 2-banded morphs displayed significantly greater decreases in preferred temperatures after treatment with naloxone than did the 5-banded morph, which showed minimal responses. It is suggested that these differences in opioid modulation of thermal preferences and behavioral thermoregulation may contribute to the polymorphic thermal preferences of natural populations of Cepaea.

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Abbreviations

B:

yellow five-banded shell type

I:

yellow two-banded shell type

U:

yellow unbanded shell type

References

  • Adler MW, Geller EB, Rosow CE, Cochin J (1988) The opioid system and temperature regulation. Ann Rev Pharmacol Toxicol 28:429–449

    Google Scholar 

  • Amit Z, Galina H (1986) Stress-induced analgesia: adaptive pain suppression. Physiol Rev 66:1091–1120

    Google Scholar 

  • Bergstrom PW, Whelan JG (1988) Effects of food and shell morph on temperature preferences of Cepaea nemoralis. Malacologia 29:341–346

    Google Scholar 

  • Burrowes WR, Assanch P, Stefano B (1983) Behavioral effects of opiates on the land snail Helix aspera. Life Sci 32:381–384

    Google Scholar 

  • Cain AJ (1983) Ecology and energetics of terrestrial molluscan populations. In: Russell-Hunter WD (ed) The Mollusca, vol 6. Academic Press, New York, pp 597–647

    Google Scholar 

  • Cameron RAD (1970) The effect of temperature on the activity of three species of helicid snail (Mollusca: Gastropoda). J Zool 162:303–315

    Google Scholar 

  • Dalton LM, Widdowson I (1989) The involvement of opioid peptides in stress-induced analgesia in the slug Arion ater. Peptides 10:9–13

    Google Scholar 

  • Frischknecht HR, Siegfried B, Waser PG (1988) Opioids and behavior: genetic aspects. Experientia 44:939–944

    Google Scholar 

  • Heath EJ (1975) Color, sunlight and internal temperature in the land snail, Cepaea nemoralis. Oecologia 19:29–38

    Google Scholar 

  • Hirst M, Kavaliers M (1987) Levorphanol but not dextrophan suppresses the foot-lifting responses to an aversive thermal stimulus in the terrestrial snail (Cepaea nemoralis). Neuropharmacology 26:121–123

    Google Scholar 

  • Innes DGL, Kavaliers M (1987) Opiates and deer mouse behavior: differences between island and mainland populations. Can J Zool 65:2504–2512

    Google Scholar 

  • Jaremovic R, Rollo CD (1979) Tree climbing by the snail Cepaea nemoralis (L.): a possible method of regulating temperature and hydration. Can J Zool 57:1010–1014

    Google Scholar 

  • Jones JS (1973) Ecological genetics and natural selection in molluscs. Science 182:546–552

    Google Scholar 

  • Jones JS (1982) Genetic differences in individual behavior associated with shell polymorphism in the snail, Cepaea. Nature 298:749–750

    Google Scholar 

  • Jones JS, Leith BH, Rawlings P (1977) Polymorphism in Cepaea: a problem with too many solutions. Annu Rev Ecol Syst 8:109–143

    Google Scholar 

  • Jones JS, Selander RK, Schnell GL (1980) Patterns of morphological and molecular polymorphism in the land snail Cepaea nemoralis. Biol J Linn Soc 14:359–387

    Google Scholar 

  • Kavaliers M (1982) Pineal mediation of the thermoregulatory and behavioral activating effects of β-endorphin. Peptides 3:379–385

    Google Scholar 

  • Kavaliers M (1989) Polymorphism in opioid modulation of the thermal responses of the land snail Cepaea nemoralis. Can J Zool 67:2721–2724

    Google Scholar 

  • Kavaliers M, Hirst M (1984) The presence of an opioid system mediating behavioral thermoregulation in the terrestrial snail, Cepaea nemoralis. Neuropharmacology 23:1285–1289

    Google Scholar 

  • Kavaliers M, Hirst M (1986) Evolutionary aspects of opiate involvement in thermoregulation. In: Stefano GB (ed) Handbook of comparative opioid and related neuropeptide mechanisms, vol 1. CRC Press, Boca Raton, Fla., USA, pp 139–152

    Google Scholar 

  • Kavaliers M, Ossenkopp K-P (1991) Opioid systems and magnetic field effects in the land snail, Cepaea nemoralis. Biol Bull 180:301–309

    Google Scholar 

  • Kavaliers M, Hirst M, Teskey GC (1983) A functional role for an opiate system in snail thermal behavior. Science 220:99–101

    Google Scholar 

  • Kavaliers M, Courtenay S, Hirst M (1984) Opiates influence behavioral thermoregulation in the curly-tailed lizard (Leiocephalus carinatus). Physiol Behav 32:221–224

    Google Scholar 

  • Kavaliers M, Hirst M, Teskey GC (1985a) The effects of opioid and FMRF-amide peptides on thermal behavior in the snail. Neuropharmacology 24:621–626

    Google Scholar 

  • Kavaliers M, Hirst M, Teskey GC (1985b) Opioid systems and feeding in the slug, Limax maximus: similarities to and implications for mammalian feeding. Brain Res Bull 14:681–685

    Google Scholar 

  • Kream RM, Zukin RS, Stefano GB (1980) Demonstration of two classes of opiate binding sites in the nervous tissue of the marine mollusc, Mytilus edulis. J Biol Chem 225:9218–9224

    Google Scholar 

  • Leung MK, Stefano GB (1984) Isolation and identification of enkephalins in pedal ganglia of Mytilus edulis (Mollusca). Proc Nat Acad Sci USA 81:955–958

    Google Scholar 

  • Leung MK, Stefano GB (1987) Comparative neurobiology of opioids in invertebrates with special atteniton to senescent alterations. Prog Neurobiol (Oxford) 28:131–159

    Google Scholar 

  • Leung MK, Boer HH, van Minnen J, Lundy J, Stefano GB (1990) Evidence for an enkephalinergic system in the nervous system of the pond snail, Lymnaea stagnalis. Brain Res 531:66–71

    Google Scholar 

  • Martin WR (1984) Pharmacology of opioids. Pharmacol Rev 35:283–323

    Google Scholar 

  • O'Neill JB, Pert CB, Ruff MR, Smith CC, Higgins WJ, Zisper B (1988) Identification and characterization of the opiate receptor in the ciliated protozoa, Tetrahymena. Brain Res 450:303–315

    Google Scholar 

  • Richards AV, Murray J (1975) The relation of phenotype to habitat in an introduced colony of Cepaea nemoralis. Heredity 34:128–133

    Google Scholar 

  • Richardson AMM (1974) Differential climatic selection in natural population of land snail Cepaea nemoralis. Nature 247:572–573

    Google Scholar 

  • Richardson AMM (1975) Energy flux in a natural population of the land snail, Cepaea nemoralis L. Oecologia 19:141–164

    Google Scholar 

  • Santoro C, Hall LM, Zukin MS (1990) Characterization of two classes of opioid binding sites in Drosophila melanogaster head membranes. J Neurochem 54:164–170

    Google Scholar 

  • Singh SM (1981) Polymorphism in colonies of the land snail Cepaea nemoralis at London, Ontario: changes over three decades. Can Field Nat 95:192–197

    Google Scholar 

  • Smith LH Jr (1981) Quantified aspects of pallial fluid and its affect on the duration of locomotor activity in the terrestrial gastropod (Triodopsis albolarbis). Physiol Zool 54:407–414

    Google Scholar 

  • Spencer RL, Hruby VJ, Burks TF (1988) Body temperature response profiles for selective mu, delta and kappa opioid agonists in restrained and unrestrained rats. J Pharmacol Exp Ther 246:92–101

    Google Scholar 

  • Spencer RL, Hruby VJ, Burks TF (1990) Alteration of thermoregulatory set point with opioid agonists. J Pharmacol Exp Ther 252:696–705

    Google Scholar 

  • Stefano GB (1982) Comparative aspects of opioid-dopamine interaction. Cell Mol Neurobiol 2:167–178

    Google Scholar 

  • Stefano GB (1989) Role of opioid neuropeptides in immunoregulation. Prog Neurobiol (Oxford) 33:149–153

    Google Scholar 

  • Steigen AL (1979) Temperature effects on energy metabolism in banded and unbanded morphs of the snail Cepaea hortensis. Oecologia 41:163–174

    Google Scholar 

  • Tilling SM (1983) An experimental investigation of the behavior and mortality of artificial and natural morphs of Cepaea nemoralis (L.). Biol J Linn Soc 19:35–50

    Google Scholar 

  • Wolda H (1965) Some preliminary observations on the distribution of the various morphs within natural populations of the polymorphic land snail Cepaea nemoralis (L.). Arch Neerl Zool 16:280–292

    Google Scholar 

  • Wong M, Gelperin A, Delaney K (1991) Opiate agonists activate feeding in Limax: comparisons of in vivo and in vitro effects. Behav Neurosci 105:15–24

    Google Scholar 

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Authors and Affiliations

  1. Division of Oral Biology, Faculty of Dentistry, University of Western Ontario, N6A 5C1, London, Ontario, Canada

    Martin Kavaliers

  2. Department of Psychology, University of Western Ontario, N6A 5C1, London, Ontario, Canada

    Martin Kavaliers

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Kavaliers, M. Opioid systems, behavioral thermoregulation and shell polymorphism in the land snail, Cepaea nemoralis . J Comp Physiol B 162, 172–178 (1992). https://doi.org/10.1007/BF00398344

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