Abstract
Pinealectomy or radical sham pinealectomy were performed on adult golden-mantled ground squirrels,Spermophilus (=Citellus) lateralis, approximately 1 month prior to the date of normal winter emergence. The first hibernatory period and subsequent active season were not different in either of the operated groups from intact animals. However, although the initiation of the second hibernatory period was not affected in the pinealectomized animals, this group failed to show the progressive increase in the length of heterothermic bouts that is characteristic of normal hibernation. Also, terminal arousal occurred approximately 6 weeks earlier in the second year after pinealectomy. Male squirrels showed a corresponding time compression in their annual gonadal cycle, as was assessed by testicular state.
These results suggest that the pineal gland of the golden-mantled ground squirrel is involved in the expression of the annual hibernatory cycle. In the absence of the pineal gland the adult of this species is unable to sustain the normal depth and duration of hibernation in the second over-wintering period following pinealectomy.
We have carried out additional experiments with young, laboratory-bornS. lateralis and with field-caught, adultS. richardsonii. The results of these studies also are described in this paper.
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BECKMAN, A. L., and SATINOFF, E. (1972): Arousal from hibernation by intrahypothalamic injections of biogenic amines in ground squirrels. Am. J. Physiol., 222: 875–879.
BENSON, B., LARSEN, B. R., and FINDELL, P. R. (1981): Melatonin and other pineal products. In, Melatonin: Current Status and Perspectives, N. Birau and W. Schloot, eds., Pergamon Press, Oxford, pp. 55–64.
DAVIS, D. E. (1976): Hibernation and circannual rhythms of food consumption in marmots and ground squirrels. Quart. Rev. Biol., 51: 477–514.
ELLIS, L., and BALPH, D. F. (1976): Age and seasonal differences in the synthesis and metabolism of testosterone by testicular tissue and pineal HIOMT activity in Uinta ground squirrels (Spermophilus armatus). Gen. Comp. Endocrinol., 28: 42–51.
GLASS, J. D., and LYNCH, G. R. (1982): Evidence for abrain site of melatonin action in the white-footed mouse,Peromyscus leucopus.Neuroendocrinology, 34: 1–6.
GWINNER, E., and DITTAMI, J. (1980): Pinealectomy affects the circannual testicular rhythm in European starlings (Sturnus vulgaris). J. Comp. Physiol., 136: 345–348.
HAGELSTEIN, K. A., and FOLK, G. E., Jr. (1979): Effects of photoperiod, cold acclimation and melatonin on the white rat. Comp. Biochem. Physiol. 62C: 225–229.
HAIM, A., and BORUT, A. (1978): The response of cold sensitive golden spiny mouse (Acomys russatus) to melatonin. J. Therm. Biol., 3: 100.
HARLOW, H. J., PHILLIPS, J. A., and RALPH, C. L. (1980): The effect of pinealectomy on hibernation in two species of seasonal hibernators,Citellus lateralis andC. richarsonii. J. Exper. Zool., 213: 301–303.
HARLOW, H. J., DARNELL, D. K., and PHILLIPS, J. A. (1982): Pinealectomy in ground squirrels: effect on behavioral and physiological responses to heat stress. Physiol. Behav., 28: 501–504.
HEATH, H. W., and LYNCH, G. R. (1981): Effects of 18 weeks of daily melatonin injection on reproduction and temperature regulation in the mouse,Peromyscus leucopus. J. Exper. Zool., 216: 193–195.
HELDMAIER, G., and HOFFMAN, K. (1974): Melatonin stimulates growth of brown adipose tissue. Nature (Lond.), 247: 224–225.
HELDMAIER, G., STEINLECHNER, S., RAFAEL, J., and VSIANSKY, P. (1981): Photoperiodic control and effects of melatonin on nonshivering thermogenesis and brown adipose tissue. Science, 212: 917–919.
HOFFMAN, R. A., and REITER, R. J. (1965): Rapid pinealectomy in hamsters and other small rodents. Anat. Rec. 153: 19–22.
LEGAIT, H., CONTET-AUDONNEAU, J.-L., and SIRJEAN, D. (1974): Données morphométriques sur quelques organes glandulaires intracraniens du loir (Glis glis). Bull. Assoc. Anat., 58: No. 161, 5 pp.
LEGAIT, H., LEGAIT, E., and CONTET-AUDONNEAU, J. L. (1974): Données morphométriques de l'épiphyse, de l'organe subfornical et du noyau supra-optique du Muscardin au cours du cycle annuel comparées à celle du Loir et du Lérot. Compt. rendus séances Soc. Biol., 168: 834.
LYNCH, G. R., and EPSTEIN, A. L. (1976): Melatonin induced changes in gonads, pelage, and thermogenic characters in the white-footed mouse,Peromyscus leucopus. Comp. Biochem. Physiol. 53C: 67–68.
LYNCH, G. R., SULLIVAN, J. K., and GENDLER, S. L. (1980): Temperature regulation in the mouse,Peromyscus leucopus: Effects of various photoperiods, pinealectomy, and melatonin administration. Int. J. Biometeor. 24: 49–55.
LYNCH, G. R., WHITE, S. E., GRUNDEL, R., and BERGER, M. S. (1978): Effects of photoperiod, melatonin administration and thyroid block on spontaneous daily torpor and temperature regulation in the white-footed mouse,Peromyscus leucopus. J. Comp. Physiol. 125: 157–163.
MARGOLIS, D. J., and LYNCH, G. R. (1981): Effects of daily melatonin injections on female reproduction in the white-footed mouse,Peromyscus leucopus. Gen. Comp. Endocrinol., 44: 530–537.
MOORE, R. Y. (1978): Neural control of pineal function in mammals and birds. In, The Pineal Gland, I. Nir, R. J. Reiter and R. J. Wurtman, eds., Springer-Verlag, Wien, pp. 47–58.
MROSOVSKY, N. (1978): Circannual cycles in hibernators. In, Strategies in Cold: Natural Torpidity and Thermogenesis, L. C. H. Wang and J. W. Hudson, eds., Academic Press, New York, pp. 21–65.
PALMER, D. L., and RIEDESEL, M. L. (1976): Responses of the whole animal and isolated hearts of ground squirrels,Citellus lateralis, to melatonin. Comp. Biochem. Physiol. 53: 69–72.
PENGELLEY, E. T., FISHER, K. C. (1961): Rhythmical arousal from hibernation in the golden-mantled ground squirrel,Citellus lateralis tescorum. Can. J. Zool., 39: 105–120.
PETTERBORG, L. J., and REITER, R. J. (1980): Effect of photoperiod and melatonin on testicular development in the white-footed mouse,Peromyscus leucopus. J. Reprod. Fert., 60: 209–212.
PHILLIPS, J. A., and HARLOW, H. J. (1982): Long-term effectttts of pinealectomy on the annual cycle of golden-mantled ground squirrels,Spermophilus lateralis. J. Comp. Physiol., 146: 501–505.
PHILLIPS, J. A., and JAMESON, E. W., Jr. (1980): Effect of photoperiod on fat accumulation in juvenileCitellus lateralis born in captivity. Can. J. Zool., 58: 2150–2152.
POPOVA, N. K., KOLAEVA, S. G., and DIANOVA, I. I. (1975): State of the pineal gland during hibernation. Byulletin Eksperimentalnoi Biologii i Meditsiny 79: 116–117.
QUAY, W. B. (1976): Seasonal cycle and physiological correlates of pinealocyte nuclear and nucleolar diameters in the bats,Myotis lucifugus andMyotis sodalis. Gen. Comp. Endocrinol. 29: 369–375.
RALPH, C. L. (1981): Melatonin production by extra-pineal tissues. In, Melatonin: Current Status and Perspectives, N. Birau and W. Schloot, eds., Pergamon Press, Oxford, pp. 35–46.
RALPH, C. L., FIRTH, B. T., GERN, W. A., and OWENS, D. W. (1979): The pineal complex and thermoregulation, Biol. Rev., 54: 41–72.
REIER, R. J. (1978): Interaction of photoperiod, pineal and seasonal reproduction as exemplified by findings in the hamster. Prog. Reprod. Biol. 4: 169–190.
REITER, R. J. (1980): The pineal and its hormones in the control of reproduction in mammals. Endocr. Rev., 1: 109–131.
ROLLAG, M. D., and NISWENDER, G. D. (1976): Radioimmunoassay of serum concentrations of melatonin in sheep exposed to different lighting regimes. Endocrinology, 98: 482–489.
SHARP, D. C., VERNON, M. W., and ZAVY, M. T. (1979): Alteration of seasonal reproductive patterns in mares following superior cervical ganglionectomy J. Reprod. Fert., Suppl. 27, 87–93.
SMIT-VIS, J. H. (1972): The effect of pinealectomy and of testosterone administration on the occurrence of hibernation in adult male golden hamsters. Acta Morphol. Neerl. Scand., 10: 269–282.
SOKOL, R. R., and ROHLF, F. J. (1969): The principles and practices of statistics in biological research. W. H. Freeman, San Francisco.
SPAFFORD, D. C., and PENGELLEY, E. T. (1971): The influence of the neurohumor serotonin on hibernation in the golden-mantled ground squirrel,Citellus lateralis. Comp. Biochem. Physiol., 38A: 239–250.
TAMARKIN, K., HOLLISTER, C. M., LEFEBVRE, N. G., and GOLDMAN, B. D. (1977): Melatonin induction of gonadal quiescence in pinealectomized Syrian hamsters. Science, 198: 953–955.
WRAGG, L. E. (1967): Effects of pinealectomy in the newborn female rat. Am. J. Anat. 120: 391–407.
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Ralph, C.L., Harlow, H.J. & Phillips, J.A. Delayed effect of pinealectomy on hibernation of the golden-mantled ground squirrel. Int J Biometeorol 26, 311–328 (1982). https://doi.org/10.1007/BF02219502
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DOI: https://doi.org/10.1007/BF02219502