Abstract
To determine the existence of preabsorptive reflex responses in fish, plasma glucose, insulin and glucagon were measured in striped bass (Morone saxatilis) pre-feeding (baseline: 0 min) and at five times post-feeding (5, 10, 20 and 40 min) following a 15 h fast. Two diets were fed, a basal agar-gel diet, and the agar-gel diet supplemented with a previously identified feeding stimulant mixture comprised of L-alanine, L-serine, betaine and inosine-5′-monophosphate at equimolar concentrations (0.1 mol l). After 11 days, blood samples were obtained from the caudal vein. In fish fed the stimulant diet, plasma insulin increased at 5 and 10 min post-feeding but fish fed the basal diet had lower levels than baseline after 5, 10 and 20 min. Glucagon levels were increased in fish fed the stimulant diet at 0–10 min post-feeding, then decreased to levels similar to fish fed the basal diet. Glucose levels were elevated in both treatments post-feeding and were similar in both treatments. These results indicate that there is an early phase of reflex insulin and glucagon secretion in fish, shortly after the beginning of a meal, as has been described in mammals and birds. Furthermore, feed palatability may play an important role in insulin and glucagon secretion.
This is a preview of subscription content, access via your institution.
References
Ahren, B. 2000. Autonomic regulation of islet hormone secretionimplications for hormonal disease. Diabetologia 43: 393–410.
Bassett, J.M. 1974. Early changes in plasma insulin and growth hormone levels after feeding in lambs and adult sheep. Aust. J. Biol. Sci. 27: 157–166.
Bellisle, F., Louis-Sylvestre, J., Demozay, F., Blazy, D. and LeMagnen, J. 1983. Reflex insulin response associated to food intake in human subjects. Physiol. Behav. 31: 515–521.
Bellisle, F., Louis-Sylvestre, J., Demozay, F., Blazy, D. and Le Magnen, J. 1985. Cephalic phase of insulin secretion and food stimulation in humans: a new perspective. Am. J. Physiol. 249 (Endocrinol. Metab. 12): E639–E645.
Berthoud, H.R., Bereiter, D.A., Trimble, E.R., Siegel, E.G. and Jeanrenaud, B. 1981. Cephalic phase, reflex insulin secretion: neuroanatomical and physiological characterization. Diabetologia 20: 393–401.
Berthoud, H.R. and Jeanrenaud B. 1982. Sham feeding induced cephalic phase insulin release in the rat. Am. J. Physiol. 242 (Endocrinol. Metab. 5): E280–E285.
Berthoud, H.R. and T. Powley. 1990. Identification of vagal preganglionics that mediate cephalic phase insulin response. Am. J. Physiol. 258 (Regulatory Integrative Comp. Physiol. 27): R523–R530.
Bruce, D.G., Chisholm, D.J., Storlein, L.H. and Kraegen, E.W. 1988. Physiological importance of deficiency in early prandial insulin secretion in non-insulin dependent diabetics. Diabetes 37: 736–744.
Calles-Escandon, J. and Robbins, D.C. 1987. Loss of early phase of insulin release in humans impairs glucose tolerance and blunts thermic effect of glucose. Diabetes 36: 1167–1172.
Carneiro, N.M., Navarro, I., Gutierrez, J. and Pliseskaya, E.M. 1993. Hepatic extraction of circulating insulin and glycogen in brown trout (Salmo trutta fario) after glucose and arginine injection. J. Exp. Zool. 267: 416–422.
Chisholm, C.J., Young, J.D. and Lazarus, L. 1969. The gastrointestinal stimulus to insulin release. I. Secretin. J. Clin. Invest. 48: 1453–1459.
De Jong, A., Strubbe, J.H. and Steffens, A.B. 1977. Hypothalamic influence on insulin and glycogen release in the rat. Am. J. Physiol. 233 (Endocrinol. Metab. Gastrointest. Physiol. 2): E380–E388.
Diamond, P. and LeBlanc, J. 1987. Role of automomic nervous system in postprandial thermogenesis in consious dogs. Am. J. Physiol. 252 (Endocrinol. Metab. Gastrointest. Physiol. 6): E719–E726.
Eilertson, C.D., Carneiro, N.M. and Sheridan, M.A. 1991. Effects of galanin, cholecystokinin, and neuropeptide-Y on pancreatic somatostatin release from cultured islets. Am. Zool. 31: 55A.
Fange, R. and Grove, D. 1979. Digestion. In: Fish Physiology. pp. 162–260. Edited by Hoar, W.S., Randall, D.J. and Brett, J.R. Academic Press, New York.
Fischer, U., Hommel H., Ziegler, M. and Jutzi, J. 1972a. The mechanism of insulin secretion after oral glucose administration. III: Investigations on the mechanism of a reflectoric insulin mobilization after oral stimulation. Diabetologia 8: 385–390.
Fischer, U., Hommel, H., Ziegler, M. and Michael, R. 1972b. The mechanism of insulin secretion after oral glucose administration. I: Multi phasic course of insulin mobilization after oral administration of glucose in conscious dogs. Differences to the behavior after intravenous administration. Diabetologia 8: 104–110.
Giduck, S.A., Theatte R.M., Kare, M.R. 1987. Cephalic reflexes: their role in digestion and possible roles in absorption and metabolism. J. Nutr. 117: 1191–1196.
Gutierrez, J., Carrillo, M., Zanuy, S. and Planas, J. 1984. Daily rhythms of insulin and glucose levels in the plasma of sea bass Dicentrarchus labrax after experimental feeding. Gen. Comp. Endocrinol. 55: 393–397.
Harmon, J.S., Eilertson, C.D., Sheridan, M.A. and Plisetskaya, E.M. 1991. Insulin suppression is associated with hypersomatostatinemia and hyperglucagonemia in glucose-injected rainbow trout. Am. J. Physiol. 261 (Regulatory Integrative Comp. Physiol. 3): R609–R613.
Hemre, G.I., O. Lie, G. Lambertsen, and A. Sundby. 1990. Dietary carbohydrate utilization in cod (Gadus Morhua). Hormonal response of insulin, glycogen and glycogen-like-peptide to diet and starvation. Comp. Biochem. Physiol. 97A: 41–44.
Hommel, H., Fischer, U., Retzlaff, L. and Knofler, H. 1972. The mechanism of insulin secretion in conscious dogs bearing fistulas of the digestive tract by sham feeding of glucose or tap water. Diabetologia 8: 111–116.
Ince, B.W. 1980. Amino acid stimulation of insulin secretion from the in situ perfused eel pancreas; modification by somatostatin, adrenalin and theophylline. Gen. Comp. Endocrinol. 40: 275–282.
Ince, B.W. 1983. Secretin-stimulated insulin release in vivo in European eels, Anguilla anguilla L. J. Fish Biol. 22: 259–263.
Ionescu, E., Rohner-Jeanrenaud, F., Proietto, J., Rivest, R.W. and Jeanrenaud, B. 1988. Taste-induced changes in plasma insulin and glucose turnover in lean and genetically obese rats. Diabetes 37: 773–779.
Karmann, H., Rideau, N., Zorn, T., Malan, A. and Le Maho, Y. 1992. Early insulin response after food intake in geese. Am. J. Physiol. 263 (Regulatory Integrative Comp. Physiol. 32): R782–R784.
Kraegen, E.W., Chisholm, D.J. and McNamara, M.E. 1981. Timing of insulin delivery with meals. Horm. Metab. Res. 13: 365–367.
Le Drean, G., Le Huerou-Luron, I., Chayvialle, J.A., Philouze-Rome, V., Gestin, M., Bernard, C., Toullec, R. and Guilloteau, P. 1997. Kinetics of pancreatic exocrine secretion and plasma gut regulatory peptide release in response to feeding in preruminant and ruminant calves. Comp. Biochem. Physiol. 117A: 245–255.
Louis-Sylvestre, J. 1976. Preabsorptive insulin release and hypoglycemia in rats. Am. J. Physiol. 230: 56–60.
Louis-Sylvestre, J. 1978. Relationship between two stages of prandial insulin release in rats. Am. J. Physiol. 235 (Endocrinol. Metab. Gastrointest. Physiol. 4): E103–E111.
Louis-Sylvestre, J. and Le Magnen, J. 1980. Palatability and preabsorptive insulin release. Neurosci. Biobehav. Rev. 4: Suppl 1, 43–46.
Lucas, F., Bellisle, F. and Di Maio, A. 1987. Spontaneous insulin fluctuations and the preabsorptive insulin response to food ingestion in humans. Physiol. Behav. 40: 631–636.
Molinero, A., E. Gomez, J. Balasch and L. Tort. 1997. Stress by fish removal in the gilthead sea bream, Sparus aurata: A time course study on the remaining fish in the same tank. J. Appl. Aquacult. 7: 1–12.
Navarro, I., Carneiro, M.N., Parrizas, M., Maestro, J.L., Planas, J. and Gutierrez, J. 1993. Post-feeding levels of insulin and glycogen in trout (Salmo trutta fario). Comp. Biochem. Physiol. 104A: 389–393.
Navarro, I., J. Gutierrez, and J. Planas. 1995. Estimates of fish glycogen by heterologous radioimmunoassay: antibody selection and cross-reactivities. Comp. Biochem. Physiol. 110C: 313–319.
Nicholson, L.C., Woods, L.C., III, and J.G. Woiwode. 1990. Intensive culture techniques for the striped bass and its hybrids. In: Culture and Propagation of Striped Bass and its Hybrids. pp. 141–157. Edited by R.M. Harrell, J.H. Kerby and R.V. Minton. American Fisheries Society, Bethesda.
Nicolaidis, S. 1977. Sensory-neuroendocrine reflexes and their anticipatory and optimizing role on metabolism. In: Chemical Senses and Nutrition. pp. 123–140. Edited by M. Kare and O. Maller. Academic Press, New York.
Nilsson, G. and Uvnas-Wallensten, K. 1977. Effect of teasing and sham feeding on plasma glycogen concentration in dogs. Acta Physiol. Scand. 100: 298–302.
Papatryphon, E. and Soares, J.H., Jr. 2000a. The effect of dietary feeding stimulants on growth performance of striped bass, Morone saxatilis, fed a plant-feedstuff based diet. Aquaculture 185: 329–338.
Papatryphon, E. and Soares, J.H. Jr. 2000b. Identification of feeding stimulants for striped bass, Morone saxatilis. Aquaculture 185: 339–352.
Parra-Covarrubias, A., I. Rivera-Rodriguez, and A. Almaraz-Ugalde. 1971. Cephalic phase of insulin secretion in obese adolescents. Diabetes 20: 800–802.
Perez, J., Zanuy S. and Carrillo M. 1988. Effects of diet and feeding time on daily variations in plasm insulin, hepatic c-AMP and other metabolites in a teleost fish Dicentrarchus labrax L. Fish Physiol. Biochem. 5: 191–197.
Pliseskaya E. M., Buchelli-Narvaez, L.L., Hardy, R.W. and Dickhoff, W.W. 1991. Effects of injected and dietary arginine on plasma insulin levels and growth of Pacific salmon and rainbow trout. Comp. Biochem. Physiol. A 98: 165–170.
Porter, R.J. and Bassett, J.M. 1979. Early insulin release following suckling in neonatal lambs and rabbits. Diabetologia 16: 201–206.
Proietto, J., Rohner-Jeanrenaud, F., Ionescu, E. and Jeanrenaud, B. 1987. Role for the oropharynx in relation of glycemia. Diabetes 36: 791–795.
Reubush K.J. and Heath, A.G. 1997. Secondary stress responses to acute handling in striped bass (Morone saxatilis) and hybrid striped bass (Morone chrysops × Morone saxatilis). Am. J. Vet. Res. 58: 1451–1456.
Ronner P. and Scarpa, A. 1987. Secretagogues for pancreatic hormone release in the channel catfish Ictalurus punctatus. Gen. Comp. Endocrinol. 65: 354–362.
Rotllant, J. and Tort, L. 1997. Cortisol and glucose responses after acute stress by net handling in the sparid red porgy previously subjected to crowding stress. J. Fish. Biol. 51: 21–28.
SAS Institute Inc., SAS/STAT® 1996. Software: Changes and Enhancements through Release 6.11. Cary, North Carolina, 1104 pp.
Small, B.C. and Soares, Jr., J.H. 1999. Effect of dietary carbohydrate on growth, glucose tolerance, and liver composition of juvenile striped bass. N. Am. J. Aquacult. 61: 286–292.
Steffens, A.B. 1976. Influence of the oral cavity on insulin release in the rat. Am. J. Physiol. 230: 1411–1415.
Strubbe, J.H. 1992. Parasympathetic involvement in rapid mealassociated conditioned insulin secretion in the rat. Am. J. Physiol. 263 (Regulatory Integrative Comp. Physiol. 3): R615–R618.
Strubbe, J.H. and Steffens, A.B. 1975. Rapid insulin release after ingestion of a meal in the unanesthetized rat. Am. J. Physiol. 229: 1019–1022.
Sundby, A., Eliassen, K.A., Blom, A.K. and Aasgaard, T. 1991. Plasma insulin, glycogen, glycogen-like peptide and glucose levels in response to feeding, starvation and life long restricted feed ration in salmonids. Fish Physiol. Biochem. 9: 253–259.
Teff, K.L., B.E. Levin, and K. Engelman. 1993. Oral sensory stimulation in men: effects on insulin, C-peptide, and catecholamines. Am. J. Physiol. 265 (Regulatory Integrative Comp. Physiol. 34): R1223–R1230.
Teff, K.L. and Engelman, K. 1996. Palatability and dietary restraint: effect on cephalic phase insulin release in women. Physiol. Behav. 60: 567–573.
Teff, K.L. and Engelman, K. 1996. Oral sensory stimulation improves glucose tolerance in humans: effects on insulin, Cpeptide, and glycogen. Am. J. Physiol. 270 (Regulatory Integrative Comp. Physiol. 39): R1371–R1379.
Tepper, B.J. 1992. Dietary restraint and responsiveness to sensorybased food cues as measured by cephalic phase salivation and sensory specific satiety. Physiol. Behav. 52: 305–311.
Wooley, O.W. and Wooley, S.C. 1981. Relationship of salivation in humans to deprivation, inhibition and encephalization of hunger. Appetite 2: 231–250.
Yalow, R.S. and Berson, S.A. 1960. Plasma insulin concentrations in non-diabetic and early diabetic subjects: determinations by a new sensitive immuno-assay technic. Diabetes 9: 254–260.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Papatryphon, E., Capilla, E., Navarro, I. et al. Early insulin and glucagon response associated with food intake in a teleost, the striped bass (Morone saxatilis). Fish Physiology and Biochemistry 24, 31–39 (2001). https://doi.org/10.1023/A:1011123908446
Issue Date:
DOI: https://doi.org/10.1023/A:1011123908446
- cephalic phase
- preabsorptive reflexes
- palatability
- pancreatic hormones
- glycemia