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Variation of food hoarding with the estrous cycle of Syrian golden hamsters (Mesocricetus auratus)
HORMONES
AND
BEHAVIOR11,259-263 (1978)
Variation of Food Hoarding Syrian Golden Hamsters
with the Estrous Cycle of (Mesocricetus auratus)
D. Q. ESTEP,' D. L. LANIER, Department
of Psychology,
University
AND
of Florida,
D. A. DEWSBURY Gainesville,
Florida
326/l
Food hoarding was assessed in 16 adult female Syrian golden hamsters (Mesocricetus aura&s) across the stages of the estrous cycle. Results show that food hoarding is depressed on the day of behavioral estrus but does not vary among the other days of the cycle. Decreases in food hoarding appear to be correlated with high levels of estrogen and progesterone. The data are consistent with the hypothesis that food hoarding, food intake, and weight gain are controlled either by the same mechanism or by similar mechanisms in some female rodents.
Three studies have implicated the gonadal hormones in the control of food hoarding in rodents. In female laboratory rats (Rnftus no~vegicus), a relationship between the stage of the estrous cycle and food hoarding has been found (Herberg, Pye, and Blundell, 1972). In this study hoarding was suppressed during behavioral estrus, suggesting that levels of hoarding may be related to fluctuating estrogen levels. In a subsequent study, Pye and Herberg (1972) found that daily injections of estrogen or testosterone depressed hoarding in ovariectomized female rats. Nyby, Wallace, Owen, and Thiessen (1973) found that in male Mongolian gerbils castration increased hoarding, whereas administration of exogenous androgen reduced hoarding. Clearly, alterations in gonadal hormones can affect food hoarding in some rodent species. The present research was designed to extend these findings by correlating changes in food hoarding with the stage of the estrous cycle in a “natural hoarder” the Syrian golden hamster (Mesocricetus nur.n~us). Several authors (Beach, 1950; Cofer and Appley, 1964; Ross, Smith, and Woessner, 1955) have pointed out that experimental investigations of hoarding might be more profitable if “natural hoarders” were studied. Hamsters clearly fall into this category as they are known to hoard substantial quantities of grain in the wild (Murphy, 1971, 1977). Pilot work in this laboratory (1) replicated the finding of Smith and Ross (1950) that female hamsters hoard more than males and (2) suggested that ’ Now at the Department
of Psychology,
University
of Georgia, Athens, Georgia 30602.
259 0018-506X/78/0113-0259$01.00/0 Copyright @ 1978 by Academic Press. Inc. All rights of reproduction in any form reserved.
260
ESTEP, LANIER,
AND
DEWSBURY
hoarding in females may vary with the stage of the estrous cycle. In the present study the hypothesis that food hoarding in female hamsters fluctuates with the stage of the estrous cycle is systematically tested. METHODS Subjects. The subjects were 16 female Syrian golden hamsters (Mesocricetus aurutus) from the outbred stock of the Lakeview Hamster Colony. All of the animals were approximately 100 days of age at the beginning of the study. They were maintained in an air-conditioned, windowless room on a reversed 14-hr light-lo-hr dark, light-dark cycle with light onset at 1900 hr. White fluorescent lights shone during the light phase while dim red lights shone at all times. Apparatus. The hoarding apparatus used was identical to that described by Lanier, Estep, and Dewsbury (1974). There were two eight-unit batteries, each unit consisting of a 20 x 15 x 15cm living cage attached to a 60 x 15 x 15cm runway. Each living cage was separated from the runway by a sliding metal guillotine door. These living cages and runways were constructed of plywood painted flat gray and 0.25-in. hardware cloth. A 25-W red light bulb was suspended approximately 60 cm above the runways of each battery. Procedure. All animals were given 7 days adaptation to the living cages before the initiation of the experiment. Four to five pellets of Purina Laboratory Chow were available in the living cages during both adaptation and the experimental period, but not during actual testing. Water was available in the living cages at all times. Hoarding tests were conducted approximately 1 hr after the fluorescent lights went out. Food pellets were removed from the living cages just prior to the start of testing. Then 100 fresh pellets of Purina Laboratory Chow were placed in each runway at the end farthest from the living cage, the guillotine doors were lifted, and the animals were allowed free access to the runway for 30 min. At the end of this time, the guillotine doors were closed, and the food pellets in the living cages were removed and counted. Each female was then given a vaginal examination to determine the stage of the estrous cycle. The stage of the estrous cycle was defined by the nature of the vaginal discharge as described by Orsini (1961). Hoarding tests were conducted daily for 25 consecutive days. RESULTS The hoarding data for the last three 4-day estrous cycles were used to compute mean hoarding scores for each day of the cycle for each female. The stages of the estrous cycle were defined in relation to the occurrence of the postestrous discharge which is defined by Baranczuk and Greenwald (1973) as Day 1 of the cycle. The mean number of pellets hoarded on Day 1 of the cycle was 25.8 f 7.4 (*SE), for Day 2,27.4 * 8.4, for Day 3,25.9 ? 8.5, and for Day 4, 13.9
ESTRUS
AND HOARDING
IN HAMSTERS
261
+- 6.4. An analysis of variance comparing hoarding scores across the 4 days of the estrous cycle revealed a significant days effect (F = 3.96, p C 0.025). A post-hoc Newman-Keuls test (Winer, 1971)revealed that hoarding on Day 4 was significantly less than on Days 1, 2, or 3 @ < 0.05). There were no significant differences in hoarding among Days 1,2, and 3. DISCUSSION
The results show a depression in food hoarding on Day 4 of the estrous cycle, the day of behavioral estrus in female hamsters (Kent, 1968; Orsini, 1961). These data are consistent with the findings of Herberg et al. (1972) for female laboratory rats showing a decline in food hoarding on the day of estrus. These authors suggest that there may be significant relationships between food hoarding levels and levels of gonadal hormones, specifically estrogen. Such relationships are also suggested by the present data. Presented in Fig. I are hoarding scores for each of the 4 days of the
FIG. I. (a) Mean number of pellets hoarded on each day of the estrous cycle. Vertical bars represent standard errors of the mean. (b) Concurrent plasma levels of estradiol and progesterone. Estmdiol levels (from Baranczuk and Greenwald, 1973) are plotted on the left in picograms per milliliter of plasma. Progesterone levels (from Lukazewska and Greenwald, 1970) are plotted on the right in nanograms per milliliter of plasma.
262
ESTEP, LANIER, AND DEWSBURY
estrous cycle plotted along with data on estrogen and progesterone levels taken from studies by Baranczuk and Greenwald (1973) and Lukaszewska and Greenwaid (1970). As can be seen from the figure, it appears that 10~ levels of hoarding on Day 4 are correlated with high levels of estradiol and progesterone. Higher levels of hoarding appear to be correlated with low levels of estradiol and progesterone. It is of some interest to note that the present data correspond nicely with the data of Morin and Fleming (1978) on the role of gonadal hormones in the regul’ation of eating and body weight in female hamsters. Morin and Fleming found that in normally cycling females, both food intake and body weight were lowest when estrogen levels were expected to be highest. The present data show food hoarding also to be lowest at this time. This parallel is of some importance in light of the hypothesis of Nyby et al. (1973) that the mechanisms controlling food hoarding and body weight regulation in some species of rodents may be similar if not the same. If this hypothesis is correct, we would predict that as in the case of feeding and weight gain, ovariectomy should increase food hoarding and replacement of exogenous estrogen should depress food hoarding. These predictions are presently being tested. ACKNOWLEDGMENTS Supported by Grant BMS75-08656 from the National Science Foundation.
REFERENCES Baranczuk, R., and Greenwald, Cl. S. (1973). Peripheral levels of estrogen in the cyclic hamster. Endocrinology 92, 805-812. Beach, F. A. (1950). The snark was a boojum. Amer. Psychol. 5, 115-124. Cofer, C. N., and Appley, M. H. (1964). Motivation: Theory and Research. John Wiley & Sons, New York. Herberg, L. J., Pye, J. G., and Blundell, J. E. (1972). Sex differences in the hypothalamic regulation of food hoarding: Hormones versus calories. Anim. Behav. 20, 186-191. Kent, G. C., Jr. (1%8). Physiology of reproduction. In Hoffman, R. A., Robinson, P. F., and Magelhaes, H. (Eds.), The Golden Hamster: Its Biology and Use in Medical Research, pp. 119-138. Iowa State University Press, Ames, Iowa. Lanier, D. L., Estep, D. Q., and Dewsbury, D. A. (1974). Food hoarding in muroid rodents. Behuv. Biol. 11, 177-187. Lukaszewska, J. H., and Greenwald, G. S. (1970). Progesterone levels in the cyclic and pregnant hamster. Endocrinology 86, l-9. Morin, L. P., and Fleming, A. S. (1978). Variation of food intake and body weight with estrous cycle, ovariectomy. and estradiol benzoate treatment. in hamsters (Mesocricetus auratus). .I. Comp. Physiol. Psychol. 92, l-6. Murphy, M. R. (1971). Natural history of the Syrian golden hamster - A reconnaissance expedition. Amer. Zoo/. 11, 632. Murphy, M. R. (1977). Intraspecific sexual preferences of female hamsters. J. Comp. Physiol. Psycho/. 91, 1337-1346. Nyby, J., Wallace, P., Owen, K., and Thiessen, D. D. (1973). An influence of hormones on hoarding behavior in the Mongolian gerbil (Meriones unguiculutus). Horm. Behav. 4, 283-288.
ESTRUS AND HOARDING IN HAMSTERS
263
Orsini, M. W. (l%l). The external vaginal phenomena characterizing the stages of the estrous cycle, pregnancy, pseudopregnancy, lactation and the anestrous hamster, Mesocricetus auratus Waterhouse. Proc. Anim. Care Panel 11, 193-206. Pye, J. G., and Herberg, L. J. (1972). Sexual dimorphism in the hypothalamic organization of hoarding behavior. Hormones 3, 282-283. Ross, S., Smith, W. I., and Woessner, B. L. (1955). Hoarding: An analysis of experiments and trends. J. Gen. Psychol. 52, 307-326. Smith, W. I., and Ross, S. (1950). Hoarding behavior in the golden hamster (Mesocriccrus aurafus). J. Gene?. Psycho/. 77, 211-215. Winer, B. J. (1971). Statistical Principles in Experimental Design, 2nd Ed., McGraw-Hill, New York.
AND
BEHAVIOR11,259-263 (1978)
Variation of Food Hoarding Syrian Golden Hamsters
with the Estrous Cycle of (Mesocricetus auratus)
D. Q. ESTEP,' D. L. LANIER, Department
of Psychology,
University
AND
of Florida,
D. A. DEWSBURY Gainesville,
Florida
326/l
Food hoarding was assessed in 16 adult female Syrian golden hamsters (Mesocricetus aura&s) across the stages of the estrous cycle. Results show that food hoarding is depressed on the day of behavioral estrus but does not vary among the other days of the cycle. Decreases in food hoarding appear to be correlated with high levels of estrogen and progesterone. The data are consistent with the hypothesis that food hoarding, food intake, and weight gain are controlled either by the same mechanism or by similar mechanisms in some female rodents.
Three studies have implicated the gonadal hormones in the control of food hoarding in rodents. In female laboratory rats (Rnftus no~vegicus), a relationship between the stage of the estrous cycle and food hoarding has been found (Herberg, Pye, and Blundell, 1972). In this study hoarding was suppressed during behavioral estrus, suggesting that levels of hoarding may be related to fluctuating estrogen levels. In a subsequent study, Pye and Herberg (1972) found that daily injections of estrogen or testosterone depressed hoarding in ovariectomized female rats. Nyby, Wallace, Owen, and Thiessen (1973) found that in male Mongolian gerbils castration increased hoarding, whereas administration of exogenous androgen reduced hoarding. Clearly, alterations in gonadal hormones can affect food hoarding in some rodent species. The present research was designed to extend these findings by correlating changes in food hoarding with the stage of the estrous cycle in a “natural hoarder” the Syrian golden hamster (Mesocricetus nur.n~us). Several authors (Beach, 1950; Cofer and Appley, 1964; Ross, Smith, and Woessner, 1955) have pointed out that experimental investigations of hoarding might be more profitable if “natural hoarders” were studied. Hamsters clearly fall into this category as they are known to hoard substantial quantities of grain in the wild (Murphy, 1971, 1977). Pilot work in this laboratory (1) replicated the finding of Smith and Ross (1950) that female hamsters hoard more than males and (2) suggested that ’ Now at the Department
of Psychology,
University
of Georgia, Athens, Georgia 30602.
259 0018-506X/78/0113-0259$01.00/0 Copyright @ 1978 by Academic Press. Inc. All rights of reproduction in any form reserved.
260
ESTEP, LANIER,
AND
DEWSBURY
hoarding in females may vary with the stage of the estrous cycle. In the present study the hypothesis that food hoarding in female hamsters fluctuates with the stage of the estrous cycle is systematically tested. METHODS Subjects. The subjects were 16 female Syrian golden hamsters (Mesocricetus aurutus) from the outbred stock of the Lakeview Hamster Colony. All of the animals were approximately 100 days of age at the beginning of the study. They were maintained in an air-conditioned, windowless room on a reversed 14-hr light-lo-hr dark, light-dark cycle with light onset at 1900 hr. White fluorescent lights shone during the light phase while dim red lights shone at all times. Apparatus. The hoarding apparatus used was identical to that described by Lanier, Estep, and Dewsbury (1974). There were two eight-unit batteries, each unit consisting of a 20 x 15 x 15cm living cage attached to a 60 x 15 x 15cm runway. Each living cage was separated from the runway by a sliding metal guillotine door. These living cages and runways were constructed of plywood painted flat gray and 0.25-in. hardware cloth. A 25-W red light bulb was suspended approximately 60 cm above the runways of each battery. Procedure. All animals were given 7 days adaptation to the living cages before the initiation of the experiment. Four to five pellets of Purina Laboratory Chow were available in the living cages during both adaptation and the experimental period, but not during actual testing. Water was available in the living cages at all times. Hoarding tests were conducted approximately 1 hr after the fluorescent lights went out. Food pellets were removed from the living cages just prior to the start of testing. Then 100 fresh pellets of Purina Laboratory Chow were placed in each runway at the end farthest from the living cage, the guillotine doors were lifted, and the animals were allowed free access to the runway for 30 min. At the end of this time, the guillotine doors were closed, and the food pellets in the living cages were removed and counted. Each female was then given a vaginal examination to determine the stage of the estrous cycle. The stage of the estrous cycle was defined by the nature of the vaginal discharge as described by Orsini (1961). Hoarding tests were conducted daily for 25 consecutive days. RESULTS The hoarding data for the last three 4-day estrous cycles were used to compute mean hoarding scores for each day of the cycle for each female. The stages of the estrous cycle were defined in relation to the occurrence of the postestrous discharge which is defined by Baranczuk and Greenwald (1973) as Day 1 of the cycle. The mean number of pellets hoarded on Day 1 of the cycle was 25.8 f 7.4 (*SE), for Day 2,27.4 * 8.4, for Day 3,25.9 ? 8.5, and for Day 4, 13.9
ESTRUS
AND HOARDING
IN HAMSTERS
261
+- 6.4. An analysis of variance comparing hoarding scores across the 4 days of the estrous cycle revealed a significant days effect (F = 3.96, p C 0.025). A post-hoc Newman-Keuls test (Winer, 1971)revealed that hoarding on Day 4 was significantly less than on Days 1, 2, or 3 @ < 0.05). There were no significant differences in hoarding among Days 1,2, and 3. DISCUSSION
The results show a depression in food hoarding on Day 4 of the estrous cycle, the day of behavioral estrus in female hamsters (Kent, 1968; Orsini, 1961). These data are consistent with the findings of Herberg et al. (1972) for female laboratory rats showing a decline in food hoarding on the day of estrus. These authors suggest that there may be significant relationships between food hoarding levels and levels of gonadal hormones, specifically estrogen. Such relationships are also suggested by the present data. Presented in Fig. I are hoarding scores for each of the 4 days of the
FIG. I. (a) Mean number of pellets hoarded on each day of the estrous cycle. Vertical bars represent standard errors of the mean. (b) Concurrent plasma levels of estradiol and progesterone. Estmdiol levels (from Baranczuk and Greenwald, 1973) are plotted on the left in picograms per milliliter of plasma. Progesterone levels (from Lukazewska and Greenwald, 1970) are plotted on the right in nanograms per milliliter of plasma.
262
ESTEP, LANIER, AND DEWSBURY
estrous cycle plotted along with data on estrogen and progesterone levels taken from studies by Baranczuk and Greenwald (1973) and Lukaszewska and Greenwaid (1970). As can be seen from the figure, it appears that 10~ levels of hoarding on Day 4 are correlated with high levels of estradiol and progesterone. Higher levels of hoarding appear to be correlated with low levels of estradiol and progesterone. It is of some interest to note that the present data correspond nicely with the data of Morin and Fleming (1978) on the role of gonadal hormones in the regul’ation of eating and body weight in female hamsters. Morin and Fleming found that in normally cycling females, both food intake and body weight were lowest when estrogen levels were expected to be highest. The present data show food hoarding also to be lowest at this time. This parallel is of some importance in light of the hypothesis of Nyby et al. (1973) that the mechanisms controlling food hoarding and body weight regulation in some species of rodents may be similar if not the same. If this hypothesis is correct, we would predict that as in the case of feeding and weight gain, ovariectomy should increase food hoarding and replacement of exogenous estrogen should depress food hoarding. These predictions are presently being tested. ACKNOWLEDGMENTS Supported by Grant BMS75-08656 from the National Science Foundation.
REFERENCES Baranczuk, R., and Greenwald, Cl. S. (1973). Peripheral levels of estrogen in the cyclic hamster. Endocrinology 92, 805-812. Beach, F. A. (1950). The snark was a boojum. Amer. Psychol. 5, 115-124. Cofer, C. N., and Appley, M. H. (1964). Motivation: Theory and Research. John Wiley & Sons, New York. Herberg, L. J., Pye, J. G., and Blundell, J. E. (1972). Sex differences in the hypothalamic regulation of food hoarding: Hormones versus calories. Anim. Behav. 20, 186-191. Kent, G. C., Jr. (1%8). Physiology of reproduction. In Hoffman, R. A., Robinson, P. F., and Magelhaes, H. (Eds.), The Golden Hamster: Its Biology and Use in Medical Research, pp. 119-138. Iowa State University Press, Ames, Iowa. Lanier, D. L., Estep, D. Q., and Dewsbury, D. A. (1974). Food hoarding in muroid rodents. Behuv. Biol. 11, 177-187. Lukaszewska, J. H., and Greenwald, G. S. (1970). Progesterone levels in the cyclic and pregnant hamster. Endocrinology 86, l-9. Morin, L. P., and Fleming, A. S. (1978). Variation of food intake and body weight with estrous cycle, ovariectomy. and estradiol benzoate treatment. in hamsters (Mesocricetus auratus). .I. Comp. Physiol. Psychol. 92, l-6. Murphy, M. R. (1971). Natural history of the Syrian golden hamster - A reconnaissance expedition. Amer. Zoo/. 11, 632. Murphy, M. R. (1977). Intraspecific sexual preferences of female hamsters. J. Comp. Physiol. Psycho/. 91, 1337-1346. Nyby, J., Wallace, P., Owen, K., and Thiessen, D. D. (1973). An influence of hormones on hoarding behavior in the Mongolian gerbil (Meriones unguiculutus). Horm. Behav. 4, 283-288.
ESTRUS AND HOARDING IN HAMSTERS
263
Orsini, M. W. (l%l). The external vaginal phenomena characterizing the stages of the estrous cycle, pregnancy, pseudopregnancy, lactation and the anestrous hamster, Mesocricetus auratus Waterhouse. Proc. Anim. Care Panel 11, 193-206. Pye, J. G., and Herberg, L. J. (1972). Sexual dimorphism in the hypothalamic organization of hoarding behavior. Hormones 3, 282-283. Ross, S., Smith, W. I., and Woessner, B. L. (1955). Hoarding: An analysis of experiments and trends. J. Gen. Psychol. 52, 307-326. Smith, W. I., and Ross, S. (1950). Hoarding behavior in the golden hamster (Mesocriccrus aurafus). J. Gene?. Psycho/. 77, 211-215. Winer, B. J. (1971). Statistical Principles in Experimental Design, 2nd Ed., McGraw-Hill, New York.