Social dominance and reproductive success in pregnant and lactating golden hamsters (Mesocricetus auratus) under seminatural conditions

Physiology & Behavior, Vol. 44, pp. 313-319. Copyright ©Pergamon Press plc, 1988. Printed in the U.S.A.

0031-9384/88 $3.00 + .00

Social Dominance and Reproductive Success in Pregnant and Lactating Golden Hamsters (Mesocricetus auratus) Under Seminatural Conditions U. W I L L I A M H U C K , 2 R O B E R T D. L I S K A N D M A R Y V. M c K A Y D e p a r t m e n t o f Biology, P r i n c e t o n University, P r i n c e t o n , N J 08544 R e c e i v e d 8 S e p t e m b e r 1987 HUCK, U. W., R. D. LISK AND M. V. McKAY. Social dominance and reproductive success in pregnant and lactating golden hamsters (Mesocricetus auratus) under seminatural conditions. PHYSIOL BEHAV 44(3) 313-319, 1988.--Pairs of female hamsters were acclimated to seminatural enclosures and permitted to interact for brief periods on days 12-14 of gestation or on days 2-4 of lactation. In one experimental paradigm, food was provided in excess of the daily requirements while in a second, food rations were restricted. Control females were similarly housed and fed but were not exposed to another animal. Paired females readily established dominant-subordinate relationships. Dominant females successfully removed food from the subordinate females and, as a result, accumulated larger food hoards. Subordinate females gave birth to fewer pups than either dominant or subordinate animals when social interactions occurred late in pregnancy and maintained smaller litters when interactions occurred during lactation. Reductions in the fecundity of subordinate females were more pronounced when the food ration was restricted. Under ad lib feeding conditions dominant females also maintained fewer young than control animals, but when food was restricted they were more successful than the control group. Subordinate females successfully defended their burrows against intrusions by dominant animals; maternal cannibalism accounted Ibr most reductions in litter size. These results suggest that a defensible burrow and the acquisition of a lbod hoard are essential for successful reproduction in this species. Hamsters Maternal social status Maternal aggression Cannibalism

Prenatal uterine mortality Infanticide

A G O N I S T I C interactions between female golden hamsters may result in reduced implantation rates when interactions occur shortly after mating (12) and in increased fetal mortality when interactions occur late in gestation (10,35). These effects are most pronounced in subordinate females (10,35) and apparently are the result of reduced plasma progesterone levels (12). Females of this species also engage in infanticide when strange pups are placed into their home cages (26,27) or when exposed to other, lactating females with their litters (unpublished observations). Previous laboratory studies of the effects of agonistic interactions on reproductive parameters have employed prolonged periods of enforced cohabitation [e.g., (35)] and/or relatively simple testing enclosures. Insofar as field studies indicate that golden hamsters construct and defend underground burrows (24), it is possible that some effects of agonistic interaction seen under laboratory conditions are unlikely to occur in the wild. It therefore seemed appropriate to reexamine this problem using a testing paradigm more closely reflecting the natural history of this solitary species. In the present study female hamsters

Food restriction

Food hoarding

were adapted to large, complex enclosures containing a nest box with a small defensible entrance and filled with wood shavings. Guillotine doors permitted brief periods of social interaction between animals in adjoining enclosures. A further objective was to determine the relative effect of brief agonistic interactions and defensible burrows during two different periods in the reproductive process. One group of females was tested on days 12-14 of the 16-day gestation period while another group was tested on days 2-4 of lactation. It has been widely observed that the intensity of agonistic interaction between conspecifics is facilitated by food shortages [e.g., (3)]. Golden hamsters are known to hoard grain in the wild (23) and several laboratory studies suggest that an adequate food supply is critical for successful reproduction. Micelli and Malsbury (21) investigated the effect of a food hoard on the development of maternal responses in virgin females. In their study, one group of females was required to gnaw at their food through wire mesh while females of a second group could hoard food pellets in their nests. Within 10 days,

1This research was supported by National Science Foundation Grant BNS-867258 and by the Biology Department of Princeton University. 2Requests for reprints should be addressed to U. William Huck at his present address: Biology Program, Sangamon State University, Springfield, IL 62794-9243.

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HUCK, t.ISK A N D McKAY

all females with food hoards behaved maternally toward strange pups placed into their home cages whereas only 61)% of the females without food hoards showed maternal responses. The presence of a food hoard also reduced pup cannibalism in lactating females (22). Food restriction during pregnancy and/or lactation significantly reduced litter size at birth and the number o f young weaned (17). In view of the foregoing, in the present study food supplies were adjusted so that subjects received either an excess of the normal amount consumed in a day or approximately 75% of the daily requirement. The benefits of dominant social status may not be apparent unless some important resource is in short supply (34). Thus, our experimental paradigm allowed us to test the ability of the dominant female to take food from a subordinate and thereby ameliorate the potentially deleterious effects of food shortage. METHOD

Animals and Husbandry. Subjects and stud males were laboratory-born descendants o f the randomly bred L V G strain obtained from Charles River, Inc. A total of 270 multiparous females 195284 days of age (mean=233.5) were used. Each had successfully reared 1 or 2 litters before the study. The pups of the last litter were removed at least 30 days prior to this study. The 90 stud males were 145--302 days of age (mean=205.9). Each had sired at least two previous litters and was rested (no sexual contact) for at least two weeks between matings. All animals were maintained in windowless, air-conditioned rooms on a reversed 14L: 10D photoperiod (lights off at 1200 hr). Except as noted below, all animals were provided with commercial laboratory chow and water ad lib.

Apparatus The test apparatus consisted of two 122 x 122 x 40 cm Plexiglas enclosures each containing a 120×5x2 cm nest box filled with wood shavings. The nest box and a 5 × 5 cm opening near one of the top corners. Plexigias ramps covered with hardware cloth enabled animals to reach the nest box opening from the enclosure floor. Each enclosure also contained a water bottle. A guillotine door permitted access to an adjoining enclosure.

Procedure Prior to testing, females matched for body weight (__.5 g) were placed into adjoining enclosures. Control females were also placed into enclosures at this time but with no female in the adjoining area. After a 4-day habituation period, the guillotine door separating the two enclosures was opened for a 30-min observation period beginning at 13:00 hr (1 hr after the onset of the dark phase of the photoperiod). At the end of this time the females were returned to their respective enclosures and the guillotine doors closed. This procedure was repeated on three consecutive days (days 12-14 of gestation in Experiments 1A and 1B and days 2-4 of lactation in Experiments 2A and 2B). Agonistic interactions between females as well as attacks on pups and incidents of cannibalism were recorded via key pads with input in real time to an IBM-PC or Aim 45 microcomputer. Agonistic behaviors included chase, attack, fight, on-back, and tall,up [described by (7)]. A female was classified as dominant if its

chase plus attack score was at least three times higher than that of the other member of a pair, providing that a minimum of five chases and attacks was observed. At 12:50 hr (e.g., 10 min before the beginning of observations), 15 g (Experiments IA and 2A) or 7.5 g (Experiments IB and 2B) of dry chow was placed into each of the female's enclosures. Earlier work indicated that pregnant and lactating females consumed 9-13 g of food per day (unpublished data). Thus the two levels of provisioning employed in this study provided either an excess of or insufficiency of nutriment to the experimental dams. All females were weighed 4 hr before the first test and two days after the last test. Any pups and food hoarded in the the females' nest boxes were also weighed at these times. RESULTS

Experiments IA and IB: Interactions on Days 12-14 of Gestation The results of Experiments IA and IB are summarized in Table 1. Among females tested on days 12-14 o f gestation and given 15 g of food dally (Experiment 1A), there were no significant differences in maternal body weights on day 12 (immediately prior to interaction). At parturition, however, the subordinate members of the interacted pairs were 8% lighter than either the control or the dominant animals. This difference was statistically significant. All groups had food hoards of similar weight on day 12. At parturition, however. dominant animals had hoards that weighed 5 times that of their subordinate counterparts and nearly twice that of control animals. Both differences were highly significant. All control and dominant animals delivered litters while only 84% of the subordinate females did s o , X~(1)=5.58, p<0.02. Littersize at parturition was highest for the control group (mean= 13.0), significantly lower for dominant females CI 1.8) and significantly lower still for the subordinate animals (8.0). Mean pup weights were similar for all three groups, however. In Experiment lB in which animals received 7.5 g of food daily, there were no differences in maternal body weights on day 12 of gestation nor at parturition following 3 days of interaction (Table 1). On day 12 females in each group had a food hoard which weighed about 4 g. At parturition the mean weight of the food hoard had not changed appreciably for the control animals. In contrast, the mean weight of food hoarded by dominant females increased over 3-fold between day 12 of gestation and parturition (Wilcoxon signed ranks test, z=5.87, p<0.001) whereas the weight of food hoarded by subordinate females diminished significantly during the same period (z=3.77, p<0.01). At parturition dominant animals had a food hoard about 14 times heavier than their subordinate counterparts and about 3 times heavier than that of control animals (Table 1). All control and dominant females delivered litters whereas only 65% of subordinate animals delivered at least some young, Xz(1)=12.63. p <0.001. Litter size at parturition was similar for control and dominant females but about 50% smaller for subordinate animals. Likewise, mean pup weights were similar for control and dominant animals and significantly lower for subordinate females. Comparison of litter size and mean pup weight for the two conditions of food supply (15 vs. 7.5 g) indicated no significant differences between the control females receiving different amounts of food nor for the dominant females. F o r subordinate females, however, both the number of pups

MATERNAL SOCIAL STATUS AND REPRODUCTIVE SUCCESS

315

TABLE 1 MEAN(_+ SEM)BODYWEIGHT,AMOUNTOF FOODHOARDED,LITTERSIZE AND PUP WEIGHTSOF DAMSINTERACTINGBRIEFLYON DAYS 12-14 OF GESTATION Control (C)

C vs. D*

Dominant (D)

D vs. St

Subordinate (S)

S vs. C*

Experiment 1A: Ad Lib Diet Number tested Maternal body weight (g) Day 12 of gestation Parturition Food hoarded (g) Day 12 of gestation Parturition Litter size Pup weight (g)

25

25

159.2 - 2.9 136.1 _+ 2.6 29.5 42.5 13.0 2.50

ns ns

-+ 4.4 --_ 2.5 _+ 0.4 _+ 0.03

ns § ~ ns

160.8 _+ 4.7 136.4 _+ 3.5 28.7 71.8 11.8 2.48

_+ 4.9 + 6.8 _+ 0.3 _+ 0.03

25 ns ~+ ns ¶ § ns

159.8 _+ 3.1 128.0 _+ 3.0 26.9 14.4 8.0 2.46

_+ 3.8 _+ 4.6 _+ 0.5 _+ 0.02

ns

ns ¶ § ns

Experiment 1B: Restricted Diet Number tested Maternal body weight (g) Day 12 of gestation Parturition Food hoarded (g) Day 12 of gestation Parturition Litter size Pup weight (g)

20 154.7 _+ 6.6 127.6 __+_5.2 3.9 4.6 11.5 2.43

_+ 0.9 ___0.4 _+ 0.5 _ 0.03

20 ns ns ns ¶ ns ns

156.7 _+ 5.1 131.2 _+ 4.9 3.9 14.2 10.8 2.41

-+ 0.8 _+ 2.2 -+- 0.5 -4- 0.02

20 ns ~ ns ¶ ¶ $

156.0 _+ 4.5 125.9 _+ 3.7 3.8 1.1 5.7 2.25

_+ 0.7 _+ 0.6 _+ 0.7 _+ 0.05

ns ns ns § ¶ $

*Mann-Whitney U-test. tWilcoxon signed-ranks test. *p<0.05, §p<0.01, ~p<0.001, ns=not significant.

(Mann-Whitney U-test, z = 3 . i 7 , p<0.01) and mean pup weights (z=2.43, p<0.05) were reduced among animals receiving 7.5 g of food daily. Ten of 25 (40%) dominant females took food from the subordinate female's area in Experiment 1A whereas 17 of 20 (85%) dominant females took food in Experiment 1B, X2(1)=7.59, p<0.01.

Experiments 2A and 2B: Interactions on Days 2--4 of Parturition The results of Experiments 2A and 2B are summarized in Table 2. For females given 15 g of food daily (Experiment 2A), maternal body weights were similar among the three treatment groups at parturition. However, body weights recorded on day 6 (two days following interactions) indicated a significant (10%) reduction in the weight of subordinate vis-h-vis control and dominant animals. All groups had food hoards of similar weight at parturition. However, on day 6 of lactation the dominant animals had a food hoard which weighed 4 times that of subordinate females and 65% more than the control animals (Table 2). Litter size for all groups was similar at parturition but on day 6 there was a mean difference of 1 pup between control and dominant animals and a mean difference of 5 pups between dominant and subordinate females. Both of these differences were statistically significant. Mean pup weight was similar for all treatment groups at parturition but on day 6 mean pup weight of the subordinate animals was significantly lower than that of the other groups. Females receiving 7.5 g of food per day (Experiment 2B)

were similar in body weight across groups at parturition. On day 6 of lactation, however, the subordinate females weighed significantly less (about 3%) than their dominant counterparts although neither of these groups differed significantly from control animals. Females in all three treatment groups had food hoards of similar weight at parturition but on day 6 the dominant animals had a food hoard weighing 36 times that of subordinate females and 4 times that of control animals. Litter size at parturition was similar for all groups and was substantially reduced in all groups by day 6 of lactation (Table 2). However, the magnitude of the reduction was not the same for all three groups (Table 3). The percent loss was highest among subordinate females, significantly lower for the control group, and lower still among dominant animals. In all treatment groups litter size reduction was greater among females receiving 7.5 g of food per day than among those receiving 15 g (Table 3).

Aggressive Behavior in all Four Experiments The number of attacks and chases received by subordinate females (Table 4) was significantly higher under conditions of food restriction than when food was provided in excess of daily requirements (Mann-Whitney U-tests; Experiment 1A vs. 1B: z=6.15, p<0.001; Experiment 2A vs. 2B: z=4.04, p<0.001). Furthermore, there was a significant inverse correlation between the number of attacks and chases received by subordinate females and the size of their litters in 3 of the 4 experiments (Table 4). Fourteen of 25 (56%) dominant females took food from the subordinate female's area in Ex-

316

H U C K , t.ASK A N D M c K A Y TABLE 2 MEAN (± SEM) BODY WEIGHT, AMOUNT OF FOOD HOARDED, LITTER SIZE AND PUP WEIGHTS OF DAMS INTERACTING BRIE FI,Y ON DAYS 2-4 OF LACTATION

Control (C)

C vs. D*

Dominant (D)

D vs. St

Subordinate {S)

$ vs~ ('

Experiment 2A: Ad Lib Diet Number Tested Maternal body weight (g) Parturition Day 6 of lactation Food hoarded (g) Parturition Day 6 of lactation Litter size Parturition Day 6 of lactation Pup weight (g) Parturition Day 6 of lactation

25

25

139.5 ± 2.3 135.2 ± 2.0

ns ns

37.9 ± 3.0 54.6 ± 2.3

ns ns

38.2 85.1

12.7 ± 0.3 11.2 ± 0.3

ns $

2.46 ± 0.02 6.19 ± 0.02

ns ns

140.6 ± 2.3 136.7 ± 2.3

25 ns ~

139.3 ~ 2.3 122.6 :* 24

ns

± 2.7 ± 4.2

ns ¶

40.1 ± 3,5 19.7 ~ 3~3

ns q

12.9 ± 0.3 10.0 ± 0.4

ns ¶

12.8 _~ {1.4 5.3 ~ 0.5

ns §

ns §

2,46 ±: 0.02 5.01 ± 0.12

ns

2.44 ± 0.03 6.12 ± 0.08

Experiment 2B: Restricted Diet Number tested Maternal body weight (g) Parturition Day 6 of lactation Food hoarded (g) Parturition Day 6 of lactation Litter size Parturition Day 6 of lactation Pup weight (g) Parturition Day 6 of lactation

2O

20

20 132.1 ± 3.6 120.5 ± 2.1

ns ns

133.4 ± 2.8 121.1 ± 2.1

ns $

134.9 ±: 3.3 117.3 + 3.1

ns ns

5.3 ± 0.9 4.4 ± 0.8

ns ¶

5.7 ± 0.7 18.7 ± 2.8

ns ~:

5.5 ± 0.8 0.5 ± 0.2

ns §

11.6 ± 0.4 4.8 ± 0.5

ns

11.9

± 0.5 6.8 ± 0.5

ns ~!

11.6 ± 0.5 3.3 t: I.I

ns ~:

2.40 ± 0.04 5.68 ± 0.10

ns §

2.41 ± 0.04 5.61 ± 0.07

ns ns

2.42 ~ 0.04 4.60 ± 0.12

ns §

*Mann Whitney U-test. tWilcoxon signed-ranks test. *p<0.05, §p<0.01, ~p<0.0001, ns=not significant.

p e r i m e n t 2A w h e r e a s all o f the d o m i n a n t animals took food in E x p e r i m e n t 2B, Xz(1)=9.39; p < 0 . 0 0 1 . DISCUSSION

W h e n p e r m i t t e d a c c e s s to an adjoining enclosure on days 12-14 o f gestation o r days 2-4 o f lactation, female golden h a m s t e r s readily estabfished dominant-subordinate relationships. D o m i n a n t animals w e r e successful in r e m o v i n g f o o d from the subordinate f e m a l e ' s area and, as a result, a c c u m u lated significantly larger food hoards. Subordinate females g a v e birth to f e w e r pups than d o m i n a n t or control (noninteracted) animals and maintained smaller litters w h e n interactions o c c u r r e d during lactation. R e d u c t i o n s in the f e c u n d i t y o f subordinate females o c c u r r e d at b o t h levels o f f o o d supply but w e r e m o r e p r o n o u n c e d w h e n the ration was restricted. T h e s e results support the c o n t e n t i o n that food hoards are important for the a v o i d a n c e o f pup cannibalism (21,22). H o w e v e r , e v e n for the d o m i n a n t female there was a cost o f agonistic interaction with a n o t h e r female. W h e n p r o v i d e d with 15 g o f f o o d per day ( E x p e r i m e n t s t A and 2A), the litter size o f d o m i n a n t animals w a s significantly smaller than that o f control females m a t c h e d for b o d y weight and

living in similar enclosures. This latter finding supports the contention that social interaction, p e r se, can also result in r e d u c e d fecundity in hamsters (10, 12, 35). W h e n the daily f o o d ration w a s restricted to 7.5 g per day, h o w e v e r , a different pattern e m e r g e d a m o n g females int e r a c t e d on days 2--4 o f lactation ( E x p e r i m e n t 213). In this test paradigm d o m i n a n t females had sil~nTw,antly m o r e pups on day 6 than did the correspond'm~ control animals. The m o s t likely explanation for this finding is that dominant animals w e r e able to maintain larger litters as a result o f the e x t r a food obtained f r o m the h o m e areas o f subordinate females. In both test paradigms, about twice as m a n y dominant animals t o o k f o o d f r o m the subordinate female s are u n d e r the r e d u c e d f o o d c o n d i t i o n as w h e n f o o d w a s p r o v i d e d in e x c e s s o f daily r e q u i r e m e n t s . A ~ t l y ; therefore, the relative c o s t s and benefits o f high ~ c e status w e r e a function o f f o o d a v ~ . O n l y w h e n f o o d w a s relatively s c a r c e did the benefit o f " r a i d i n s " f o o d f r o m the s u b o ~ female' s h o m e a r e a o u t w e i g h the detrimental effects o f social interaction. A l t h o u g h in e a c h e x p e r i m e n t a l paradigm the guillotine d o o r was o p e n e d for 15 rain on e a c h Of 3 c o n s e c u t i v e days,

M A T E R N A L SOCIAL STATUS AND REPRODUCTIVE SUCCESS

317

TABLE 3 MEAN (-+ SEM) PERCENTREDUCTIONIN LITTERSIZE BY DAY 6 OF LACTATIONOF DAMS INTERACTINGBRIEFLY ON DAYS2-4 Daily Food Ration

Control (C)

15 g U-test* 7.5 g

11.5 -+ 1.9 ¶ 60.8 _+ 9.5

C vs. D* * ~

Dominant (D) 22.7 _+ 5.3 ¶ 41.8 _ 6.6

D vs. St

Subordinate (S)

C vs. S*

§

58.9 - 8.9

¶

¶

74.0 _+ 9.4

*

*Mann-Whitney U-test. tWilcoxon signed-ranks test. ~:p<0.05, §p<0.01, Sp<0.001.

TABLE 4 MEAN (_+ SEM) NUMBEROF ATTACKSAND CHASES RECEIVED BY SUBORDINATEFEMALESAND SPEARMANRANK CORRELATION COEFFICIENTSBETWEENAGGRESSIONSUSTAINEDBY SUBORDINATE FEMALES AND LITTER SIZE AT END OF EXPERIMENT

Experiment 1A 1B 2A 2B

Number of Attacks and Chases Received by Subordinates

Spearman rho Between Aggression Sustained and Litter Size

13.9 +__1.4 34.7 _+ 4.1 14.3 _+ 1.0 25.1 _+_1.7

-.361" -.384* -.374* -.194 ns

*p<0.05.

only a small fraction of this time was spent interacting with another animal. In fact, interaction time (defined as the two animals being within one body length of one another) varied from approximately 3.0 min per day of Experiments 1A and 2A to about 4.0 min per day in Experiments 1B and 2B. These relatively brief periods of interaction are consistent with the socioecology of solitary species (24) and suggest that the effects observed under the conditions of the present study could occur in the wild. In all four experimental paradigms dominant animals investigated the entrance of the subordinate female's burrow and started digging. In all but one case, the subordinate female was present in her burrow and started digging out toward the intruder. The subordinate animal would snap at the digging intruder and in all cases this resulted in the intruder's retreating. Thus, when the subordinate female was present in her burrow, none of the dominant animals ever reached the nest chamber. In a single case (Experiment 2B) in which the subordinate female was out of her nest collecting food and drinking water, the dominant animal dug into her nest unopposed. The intruder then killed 3 of 5 pups by biting them on the head or neck and pushed them into her cheek pouches. She then returned to her own burrow, took the pups out of her mouth, and began eating them. Although few systematic field studies of infanticidal behavior have been conducted, Hoogland's (8) 7-year study of black-tailed prairie dogs (Cynomys ludovicianus) suggests that infanticide in this species occurs under similar circumstances as those reported here. Hoogland found that infanticide was the major source of juvenile mortality and that the most common

killers were lactating females. Food deprivation increased the incidence of strange male-induced infanticide in Mongolian gerbils under laboratory conditions (4). The results of the present study show that having established a defensible burrow, female hamsters are highly successful in excluding intruders from their nest. Having been attacked outside of their burrows, many of the subordinate females did not come out to collect the daily food ration or to drink water. Thus, protection of the nest site appeared to have a higher priority than foraging for food and water. This undoubtedly led to increased cannibalism of the litter by the dam herself and (with the exception of the single case of infanticide by a dominant female described above) accounted for the significantly smaller litters of subordinate females in Experiment 2. Although maternal cannibalism and infanticide by a strange female both result in the death of offspring, the former behavior would allow subordinate females to recoup at least some of their parental investment which could then be apportioned to the remaining young or held in reserve for a subsequent breeding. Although the incidence of stranger-perpetrated infanticide was rare in the present study, one should not deduce from this that infanticide is not a major selective factor under natural conditions. Rather, it is likely that infanticide is an ever-present danger and represents a strong selective pressure for the construction of a defensible nest as well as territorial behavior in the wild [e.g., (1, 5, 9, 16, 18)]. The importance of a defensible nest site for protection of the litter has also been demonstrated for other rodents under laboratory conditions. Experiments with lemmings and house mice

318

HUCK, LISK AND McKAY

living in simple laboratory cages indicate that maternal females are unable to defend their young against intruders (2, 13, 15, 19, 20, 33, 36). In contrast, when a two-cage system is employed with cages connected by a tunnel, maternal females were able to exclude intruders in almost all trials (36). The decreased littering rates and reduced litter sizes at parturition noted in Experiments 1A and 1B are consistent with earlier reports of socially-induced fetal losses in this species (10,35). In a companion paper, Huck, Lisk, Miller and Bethel (12) found that levels of circulating progesterone (P) were significantly reduced in socially subordinated female golden hamsters following brief exposures to another female. The reduced P levels were accompanied by an increased incidence of implantation failure when social interactions occurred on days 2-4 after mating and by increased fetal mortality when interactions occurred later during pregnancy (days 5-7 or 10-12). In that study, P levels, the incidence of implantation failure, and the rate of fetal resorption were all highly correlated with the number of attacks and chases sustained by subordinate females. The latter findings were partly corroborated by the results of the Spearman rank coefficients reported in the present study (Table 4). A significant inverse correlation between the number of attacks and chases received by subordinate females and the size of their litters was noted in 3 of the 4 experimental paradigms (a similar but nonsignificant tendency was noted in the fourth). It is likely that reduced P levels in subordinate animals were an effect of social stress and that increased fetal mortality was a result of the decreased P levels [see (12)]. In certain microtine rodents (e.g., prairie voles and pine voles) introduction of a strange male can cause spontaneous abortion as late as day 17 of a 21-day pregnancy (14, 28, 31, 32). Clearly, socially-induced fetal

mortality in many species of rodents is not restricted to the implantation period or early pregnancy. All tb_ree groups o f females experiencing food restriction after parturition (Experiment 2B) manifested a decrease in litter size whereas only the subordinate animals manifested reduced litter sizes as a result of prepartum food restriction (Experiment 1B). Thus it appears that food resources become more critical during lactation. Since the golden hamster hoards grain in the wild (23,24) and food hoards have been shown to reduce the amount of normally occurring pup cannibalism (21,22), it is likely that the female normally provisions the maternal nest with the food necessary for the period of lactation. This would decrease the necessity of leaving the nest and is consistent with our finding that females subjected to disturbance by intruders tended to remain in their nest. Female hamsters hoard more food than do males (30) and a significant increase in the amount of hoarding occurs beginning on day 12 of pregnancy (6). However, female hamsters do not increase their daily food intake during pregnancy (6,37) although they do increase food intake somewhat during lactation. When placed on a deprivation food schedule, hamsters do not compensate by eating more during restricted times. Indeed, they appear incapable of such compensation since they will eventually die if food is restricted to a few hours per day. Thus feeding in the hamster is noncompensatory; they tend to eat the same number of calories per unit of time after deprivation (and weight loss) and under ad lib conditions (29). As a result, females of this species lose weight throughout lactation [e.g., (11,17)]. Given these physiological constraints as well as the unpredictable nature of the availability of resources under the semi-arid conditions in which the hamster is found in the wild (23,25) the necessity of a large and defensible food hoard for successful reproduction is apparent.

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