Differential temporal behavior between males and females in the hibernating ground squirrel, Citellus lateralis

Camp. Bwchrm. Phwol. Vol. 64A. pp. 593 to 596 0 Pergamon Press Ltd 1979 Printed in Great Bnlain

TEMPORAL BEHAVIOR BETWEEN DIFFERENTIAL MALES AND FEMALES IN THE HIBERNATING GROUND SQUIRREL, CZTELLUS LATERALIS ERIC T. PENGELLEY,R. C. ALOIA’, BRIAN M. BARNES and DOROTHY WHITSON Department of Biology, University of California, Riverside, CA 92521 and ‘Department of Anesthesiology, Loma Linda University Medical Center, Loma Linda, CA 92354, U.S.A. (Received 5 March 1979)

Abstract-l. In order to elucidate the differences in the temporal behavior between captive males and females of the hibernating ground squirrel, Citellus lateralis, animals were kept for 4yr at an ambient temperature of 5 +_ 1°C and a photoperiod of 12L/12D, with food and water ad lib. 2. Seven parameters were measured, with the following results: (1) the mortality rate of males is higher than females, (2) males hibernate less often than females, (3) the length of the heterothermic period is greater for females than males; but both sexes increase the length of this in successive years, (4) there is no difference between the sexes in the length of the free-running circannual period, provided the females do not breed, (5) the circannual body weight rhythm is dependent upon the homothermicheterothermic rhythm, or vice versa (6) males spend less time than females in hibernation during a heterothermic period, due to a shorter period, but (7) males exhibit longer continuous periods of hibernation within a whole heterothermic period. 3. The physiological and ecological significance of these differences between the sexes is discussed.

INTRODUCTION As far back as the first symposium on mammalian hibernation (Lyman & Dawe, 1960), the questions were raised as to whether males and females of a particular species of hibernators behaved differently in their temporal responses to the environment. This is an important problem for it should help to elucidate the mechanisms by which various species are adapted to such important factors as annual breeding and the alternation between heterothermic and homothermic states in the environments in which the mammals live. Subsequently it was determined that mammalian hibernators exhibit distinct periodic arousals during their heterothermic phase (Pengelley & Fisher, 1961, 1967; Pengelley & Asmundson, 1972; Pengelley 8~ Kelly, 1966; Pengelley et al., 1972; Heller 8~ Poulson, 1970; Johansson 8~ Senturia, 1972; Richter, 1978). Although the mechanism of these arousals is fairly well understood (Horwitz, 1968), the apparent physiological necessity for them is quite unknown. Additionally, they have different temporal relationships in different species (Pengelley & Kelly, 1966), and they can also be correlated temporally to the environmental temperature (Pengelley & Fisher, 1963; Pengelley et al., 1971). In addition to these periodic arousals during the heterothermic phase, many species of hibernators, including Citellus lateralis, exhibit an endogenous circannual rhythm within which they alternate between a heterothermic and homothermic state (Pengelley & Fisher, 1957; Pengelley & Kelly, 1966; Pengelley & Asmundson, 1969, 1974; Richter, 1978), and the sum of these two periods represents the free-running period of the circannual rhythm. This is a major temporal aspect in the life of the species, because to sur-

vive not only must it become heterothermic at the right time of year, but it must also become homothermic at the right time to breed. It has in fact already been demonstrated in Citellus lateralis (Pengelley & Asmundson, 1975), that female gestation and lactation are important factors as Zeitgebers in the overall circannual rhythm. Thus it seemed important to investigate the potential differences in the temporal behavior of male and female hibernators. Because of the length of the experiments (4yr), it was possible to observe accurately seven different and pertinent phenomena between males and females. These were (I) the mortality rate, (2) years when particular animals did not hibernate, (3) the length of the whole hibernation (heterothermic) period, (4) length of the circannual freerunning period, (5) the circannual body weight rhythm, (6) days spent in hibernation during the whole heterothermic period, and (7) length of continuous hibernation periods within the whole heterothermic period. MATERIALS AND

METHODS

Golden-mantled ground squirrels, Citellus later&. were trapped in September 1970, on the east side of the Sierra Nevada near Mammoth Lakes, CA, at an altitude of approx 8OOOft.They were brought to the laboratory and housed in individual cages in a room with a photoperiod of 12L/12D, and an ambient temperature of 23 + 1°C. The experiment was started on October 13, at which time 53 animals (29 males and 24 females) were transferred to an environmental chamber at an ambient temperature of 5 _+ 1°C and a photoperiod of 12L/12D. All animals in the experiment were supplied with Purina lab chow and water ad lib. They were maintained under these conditions for over 4 yr. Disturbances were kept to a minimum, but the animals were observed and maintained daily. The 593

594

ERIC T. P~NGELL~Y et u/.

hibernating (heterothermic) state was determined by the “sawdust technique” (Pengelley & Fisher. 1961). In addition accurate weight records were kept for each animal. All statistical data (where appropriate) were done using Student’s r-test (two-tailed) for significance, and data from years where there was no hibernation were excluded.

225 150 75

RESllLTS

The temporal hibernating behavior of all male and female C. latrrdis in the experiment is graphically displayed in Fig. 1. This clearly shows a higher mortality rate for males. The figure also shows that there is a greatly increased number of free-running circannual periods in which the males did not exhibit a heterothermic period, 7:l. which we take to mean that in comparison to females, males in captivity do not behave as much in conformity to what is probably their normal behavior in the wild state. This fact also agrees with other emperical knowledge (Pengelfey. personal observation). From the data used to plot Fig. I, statistical analysis reveals that females have a significantly longer hibernation period (heterothermic period) than do males (P < 0.001). but both sexes increase the length of this in successive years. The data also indicate that for those animals exhibiting a regular circannual free-running period there is no

u; L ” ” Fig. 2. Body wzght?n grzs ;brdinze) ;ottedffiover a 4 yr period (abscissa) to show coordination with homothermic and heterothermic periods. Symbols and environmental conditions as for Fig. 1.

significant statistical difference between males and females. Furthermore, it is obvious from the graph that male hibernating behavior is more irregular and less predictable than female and thus the female hibernates for a longer period of time than males. This fact but even

can be seen from inspection more striking by comparing

of the graph, females such

as 878 and 829 with males such as 964 and 876.

x

i

i

.i

Fig. I. Comparison of hibernation patterns bars represent heterothermic periods, open experiment terminated, J indicates January,

i

.i

i

j

i

i

of male and female C. latrralis over a 4 yr period. Black bars homothermic periods. x indicates death, 0 indicates A indicates August. Ambient temperature 5 + 1°C. photoperiod IZL/lZD.

Male and female hibernating

squirrels

595

Fig. 3. Comparison of daily behavior of a typical male and female throughout a whole heterothermic period. Horizontal dashes indicate hibernation at 5°C vertical arrow indicates homothermic state at 37°C. diagonal arrow indicates periodic arousal. Environmental conditions as for Fig. 1.

In Fig. 2 the changes in body weight of four animals are plotted in relation to the homothermic and heterothermic periods of the circannual free-running period. The animals plotted here were carefully chosen to exhibit specific phenomena. The female 817 and the male 784 are as near to the typical pattern of behavior for their sex as it is possible to determine. The female shows a remarkably constant rhythm of homothermy and heterothermy with a weight gain correlating to the former and a weight loss to the latter. The male homothermic and heterothermic periods are less regular, and a body weight higher than that of the female is usually maintained. Additionally, the periods of weight gain conform to a progressively more condensed homothermic period. The data for the female 827 and the male 876 clearly illustrates the fact that the correlation between the rise and fall of weight is dependent upon the homothermic heterothermic rhythm, or uice versa. Thus in the female, only in the first year is a partial homothermicheterothermic rhythm observed. In the male there was a normal correlation between weight and the homothermic-heterothermic rhythm during the first year, but an absence of both thereafter. In Fig. 3 the daily behavior of a typical male and female are compared throughout one entire heterothermic period. This figure shows the intermittent nature of hibernation. Comparison of the male and female in this figure, as well as all animals in the experiment, it is clear that males typically have longer continuous bouts of hibernation than females, with fewer arousals, but a shorter whole heterothermic period. In this figure the longest continuous bout for the male is 16 days, and for the female 9 days. However towards the end of the heterothermic period the male’s frequency of arousals increases more rapidly and it becomes homothermic sooner, which is in general typical for the species. DISCUSSION It is clear from the results of this study that there are indeed differences in the temporal behavior of male and female C. lateralis, though the biological significance of these is not as easily determined. It might appear on the surface that the generally more active and erratic temporal behavior of males is due to the influence of testosterone. However, this does

not seem to be the case since Pengelley & Kelly (1966) compared the behavior of juvenile males, which were castrated shortly after birth, with normal juvenile males, and were unable to detect any statistically significant differences. Thus it may be that the differences observed between the sexes in the experiments reported here are due to inherent biological differences between males and females. Moreover it has been shown (Pengelley & Asmundson, 1975) that females, which breed during a presumptive spring exhibit or longer free-running circannual period than males. but when no breeding takes place, as in these experiments, there is no difference in the length of the circannual period between the sexes, In other words, a nonbreeding female has the same circannual period as a male. However within this circannual period there are obviously many differences. One of these is the fact that males arouse earlier than females in the presumptive spring. This seems to have ecological significance for the same phenomena in the natural environment was observed by Hock (1955, 1956) in the alaskan ground squirrels. Presumably this is related to the biological necessities of a male finding an estrus female as soon as possible after emergence from hibernation and also to the possibility that this gives males more opportunity to mate with several females. There is also the possibility that the males’ sperm requires some period of homothermy to multiply and mature after the long period of heterothermy, most of which is spent at low body temperatures. The nature of the periodic arousals from hibernation as shown in Fig. 3 were first reported by Pengelley & Fisher (1961) and despite some considerable effort to explain the physiological necessity of these, there has been no satisfactory solution. They seem to be universal in all species of hibernators so far studied (Wong & Hudson. 1978) and we believe this must be due to some basic mammalian physiological or biochemical need which requires that the animal return to the homothermic state periodically. This seems probable to us since these arousals are expensive from an energy conservation point of view (Horwitz. 1968). In fact. by far the greater part of the body weight lost by the animal during the heterothermic period is due to the energy production from fat during these periodic arousals. In conclusion it may be said that the temporal hibernating behavior

ERIC T. PENGELLEY et al.

596 of females is more than males, which planning of future tigations of these basic physiological

stable and more easily predictable has important implications in the experiments, and that further invesaspects will inevitably produce a and ecological understanding.

Acknowledgements-This study was supported by Grant GB-40827 from the National Science foundation, and secondarily by an Intramural Grant from the University of California. We wish to thank Ms. Sally Asmundson for her dedicated technical assistance.

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