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Failure of strange females to cause pregnancy block in collared lemmings, Dicrostonyx groenlandicus
(1985)
BEHAVIORAL AND NEURAL BIOLOGY 4 4 , 4 8 5 - 4 9 1
BRIEF REPORT Failure of Strange Females to Cause Pregnancy Block in Collared Lemmings, Dicrostonyxgroenlandicus RONALD J.
BROOKS, MELODY
A.
DONALD, AND LIN SCHWARZKOPF1
Department of Zoology, University of Guelph, Guelph, Ontario N1G 2W1, Canada The effects of exposure to unfamiliar females on pregnancy success of recently mated females were examined in collared lemmings (Dicrostonyx groenlandicus). Four days after mating, females in their home cage were exposed to strange, female intruders that were either nonpregnant or 16 days pregnant. Other recently mated females were introduced to the home cage of 16-day-pregnant females. Pregnancy success of the recently mated females was not reduced in any of these treatments. In the paired encounters, there was no relationship between dominance status and pregnancy status, nor between dominance and pregnancy success. These results do not support the hypothesis that in species in which females are aggressive and readily commit infanticide, unfamiliar females should cause other females to terminate early-stage pregnancies. © 1985AcademicPress, Inc.
Although pregnancy block by strange males was discovered more than 20 years ago and has been demonstrated in many species of rodents (Labov, 1981; Schwagmeyer, 1979), there is still no widely accepted explanation of its selective value to the aborting female (Heske & Nelson, 1984; Schwagmeyer, 1979). Recently, however, some authors have proposed that pregnancy failure is an adaptive response of females to infanticidal behavior of strange males (Huck, Bracken, & Lisk, 1983; Labov, 1981; Mallory & Brooks, 1980). Thus, when a newly pregnant female encounters a strange male who is likely to kill her neonates, she should terminate the pregnancy and remate with the new male, because the new male is unlikely to kill his own offspring (Labov, 1981 ; Mallory & Brooks, 1980). This tactic confers a selective advantage because the cost to the female of termination, committed investment, and time is small for unimplanted embryos compared to loss of neonates. Recently, Huck et al. (1983) attempted to test this hypothesis using 1 Financial support was provided by NSERC Grant A5990 to R. J. Brooks. Send requests for reprints to Dr. Brooks. 485 0163-1047/85 $3.00 Copyright © 1985 by Academic Press, Inc. All rights of reproduction in any form reserved.
486
BROOKS, DONALD, AND SCHWARZKOPF
golden hamsters (Mesocricetus auratus). They reasoned that because female hamsters are more aggressive than males and because they readily kill unrelated, undefended neonates, these females should be able to terminate pregnancy in other females as readily as males do in other rodents. They found that pregnancy success was significantly reduced among recently mated females when they were defeated in encounters with other pregnant females.. In collared lemmings, Dicrostonyx groenlandicus, as in golden hamsters, females readily commit infanticide (Mallory & Brooks, 1980), and are highly aggressive (Brooks & Banks, 1973), especially toward other females. Therefore, we tested the hypothesis of Huck et al. (1983) that in such species females would abort preimplantation pregnancies when confronted by unfamiliar females. Experimental subjects were derived from lemmings trapped at Churchill, Manitoba in 1980 and 1981. They were maintained on an 18.5 L:5.5 D photoperiod at 18 + 4°C and were housed individually in opaque plastic cages (44 x 28 x 15 cm) with corn grit substrate and paper towels for nesting. Guinea pig chow (Ralston Purina) and water were provided ad libitum. Estrous, nulliparous females were paired with males and if ejaculation was observed within 30 min, females were left with the males for 24 hr, after which the male was removed. Implantation in collared lemmings occurs on Day 5 postcoitum (Hasler & Banks, 1975). All experimental females were tested 4 days after mating and are referred to as "recentlymated" females. Experiment 1. Because even fairly mild external stressors and disturbance may block pregnancy in collared lemmings (Mallory & Brooks, 1980), we tried to separate effects of such trauma from effects of the presence of strange females per se. In the first experiment, we tested whether pregnancy success of females in their home cage would be reduced when they were exposed to the odor or physical presence of a strange female. Thirty-six recently mated females were assigned randomly to one of three treatments or to a control. In Treatment 1, 200 cc of feces and soiled cage substrate from a strange, nonpregnant female and a paper towel soaked with fresh urine from the same female were introduced to the home cage of a recently mated female. In Treatment 2, a sexually mature, nonpregnant, nonlactating female, previously housed in another room, was introduced into the home cage of the experimental female. Frequency of attack, bite, mount, tooth chatter, and initiation of boxing was recorded for 15 min. Behavioral acts were defined as in Brooks and Banks (1973). The intruder female was removed after 24 hr. In Treatment 3, a 16-daypregnant female was introduced into the home cage of a recently mated female. Behavior was recorded as in Treatment 2. Intruders were removed after 4 hr to reduce mortality. In a control treatment, clean substrate
P R E G N A N C Y SUCCESS IN LEMMINGS
487
and a paper towel were added to the home cage of a recently mated female. The purpose of Treatments 2 and 3 was to expose experimental females to relatively unaggressive (nonpregnant) females and to females in late gestation that we expected to be more aggressive than the recently mated experimental females (Huck et al., 1983). Experiment 2. In this experiment, we tested the hypothesis that females would terminate pregnancy when they encountered an aggressive, strange female in the latter's home area. Nineteen recently mated females were assigned randomly to a treatment and a control. In Treatment 1, recently mated females were introduced into a 16-day-pregnant female's home cage. Behavior was recorded for 15 min as in Experiment 1, after which the recently mated females were removed immediately to prevent serious injury and returned to their home cage. In the control, recently mated females were picked up and placed in a clean unoccupied cage and returned to their home cage after 15 min. Following all treatments, females were left in their home cages for the remainder of gestation. At parturition, date of birth and litter size were recorded. In all experiments, if the 16day-pregnant female failed to give birth, we did not use the data involving that female as we could not be certain she was pregnant at the time of the encounter. In Experiment 1, there was no significant difference between the number of females having litters in the control versus the other three treatments (X2(3) = 1 . 5 5 , p > .05). Similarly, mean litter sizes among treatments were the same [ANOVA F(3, 27) = 0.834, p > .05 (Table 1)]. In T r e a t m e n t 2, recently mated resident females attacked and bit nonpregnant intruders more often than the intruders attacked and bit residents, but there were no differences between the two groups in frequency of o c c u r r e n c e of the remaining behavior patterns measured (Table 2). There was great variation in behavioral response during the encounters. F o r example, 3 of 10 intruder females died during or shortly after the encounters, whereas in 2 of 10 pairings none of the five measured behavior patterns occurred. In T r e a t m e n t 3, recently mated resident females were more likely to bite than were 16-day-pregnant intruders (Table 2). There were no significant differences between these two groups in any of the other measured patterns of behavior. H o w e v e r , some females were badly injured in both groups. In E x p e r i m e n t 2, there was no significant difference in pregnancy rate between treatment and control groups [Xz(1) = 0.114, p > .05 (Table 1)]. No significant differences occurred between 16-day-pregnant (home cage) and recently mated females in frequency of any measured behavior patterns (Table 2). Recently mated females that subsequently had a litter attacked 16-daypregnant females in the latter's home cage 39.0 +_ 24.1 (mean + SD)
488
BROOKS, DONALD, AND SCHWARZKOPF
TABLE 1 Number of Successful Pregnancies and Mean Litter Size (± SD) in Each Treatment Group in Experiments 1 and 2 Sample size
Number of successful pregnancies
Mean litter size
Treatment 1 Recently mated female and soiled cage substrate
10
8
3.0 + 1.5
Treatment 2 Recently mated female and nonpregnant female
10
7
3.6 -4- 2.9
6
6
2.2 --- 0.8
10
9
3.2 --- 0.8
9
6
3.0 _+ 1.6
10
7
3.0 ± 2.1
Group Experiment 1
Treatment 3 Recently mated female (home cage) and 16-day-pregnant female Control Recently mated female and clean bedding Experiment 2
Treatment 1 16-Day-pregnant female (home cage) and recently mated female Control Recently mated female into strange cage
t i m e s p e r e n c o u n t e r (n = 6). T h o s e t h a t s u b s e q u e n t l y f a i l e d to h a v e a l i t t e r a t t a c k e d 64.7 ___ 22.5 t i m e s p e r e n c o u n t e r (n = 3). This d i f f e r e n c e w a s n o t significant (t(7) = 1.36, p > .05). I n b o t h i n s t a n c e s , r e c e n t l y mated intruders attacked more often than did their 16-day-pregnant resident o p p o n e n t s (21.5 _+ 16.7 a n d 51.0 --_ 22.1 a t t a c k s , r e s p e c t i v e l y , f o r t h e latter). H o w e v e r , neither o f these differences was significant (when r e c e n t l y m a t e d f e m a l e s d e l i v e r e d a litter; t(5) = 1.26, p > .05; w h e n r e c e n t l y m a t e d f e m a l e s d i d n o t d e l i v e r a litter, t(2) = 0.549, p > .05). T h e r e f o r e , t h e r e w a s n o t e n d e n c y f o r s u b o r d i n a t e b e h a v i o r in r e c e n t l y m a t e d f e m a l e s to b e a s s o c i a t e d w i t h p r e g n a n c y failure, n o r w a s t h e r e a n y t e n d e n c y f o r
PREGNANCY SUCCESS IN LEMMINGS
489
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g +1 +1 +1 ÷1 +1 0 e~
A
+1 +1 +1 ÷1 +1 ©
0
o+ i
o
.~
+1 +1 ÷1 ÷1 +1
.3
~,~ v
~ve ÷1 +1 ÷1 +1 41
d ~ d d 0
÷1
~+.' ~2 .+~1 2 +'
o+
÷1 +1 ÷1 +1 +1 e~
. ~ o
490
BROOKS, DONALD, AND SCHWARZKOPF
females in advanced stages of pregnancy to dominate recently mated females. Recently mated female lemmings terminate pregnancy when exposed to strange males or even to repeated gentle handling (Mallory & Brooks, 1980). Furthermore, female rodents abort more readily when younger (e.g., Chipman & Fox, 1966) and when nulliparous (Clulow, Franchetto, & Langford, 1982), and our recently mated females were young and nulliparous. In addition, females apparently can cause other females to block in hamsters (Huck et al., 1983) and in mice (Yamazaki, Beauchamp, Wysocki, Bard, Thomas, & Boyse, 1983). Nevertheless, our results indicated that neither odor nor presence of strange females in the home cage or in an unfamiliar cage terminate preimplantation pregnancy in collared lemmings. As expected, recently mated (usually pregnant) females were aggressive, and usually defeated nonpregnant intruders. However, no clear dominance emerged between recently mated and 16-day-pregnant females, although the former bit more often when in their home cage. Therefore, our results do not support the hypothesis that in rodents in which females are aggressive and likely to commit infanticide, females should also be able to induce abortion in other females. This result would also appear not to support the hypothesis that potential infanticide is a selective force that makes pregnancy block adaptive for a female confronted by a novel conspecific. However, even if female lemmings did terminate pregnancy after encountering a strange female, as hamsters apparently do (Huck et al., 1983), this would not constitute strong support for this hypothesis. Females may avoid infanticide when confronted by a strange male by terminating pregnancy and remating with the strange male. In contrast, females that terminate pregnancy when confronted by a strange female will gain nothing. They can probably remate because males are usually available (Brooks & Banks, 1973), but even if they do remate, the new litter may still be susceptible to the intruder female. Hence, while the hypothesis is logical for male intruders (Labov, 1981; Mallory & Brooks, 1980), it is not for female intruders (Huck et al., 1983). We suggest that the results of Huck et al. (1983) may be explained more parsimoniously as the result of physical trauma suffered by subordinate females. In lemmings, this trauma was apparently insufficient to terminate pregnancy. In fact, recently mated females tended to be more aggressive than 16-day-pregnant females, but even when they "lost" in the experimental encounter, two out of three still gave birth. In addition, although it did not emerge clearly in our study, in nature, female lemmings at their homesites are likely to dominate intruders of either sex (Brooks & Banks, 1973). This is probably true for most rodents. Females on homesites are unlikely to terminate pregnancy because of losing a conflict. Pregnancy termination in response even to strange males has been
PREGNANCY SUCCESS IN LEMMINGS
491
documented only in the laboratory. Perhaps future consideration of its selective value should involve a serious attempt to integrate laboratory work on chemosensory recognition (Yamazaki et al., 1983) with some pertinent field data on population structure and density (Heske & Nelson, 1984). At present, such data are lacking. REFERENCES Brooks, R. J., & Banks, E. M. (1973). Behavioural biology of the collared lemming Dicrostonyx groenlandicus (Traill): An analysis of acoustic communication. Animal Behaviour Monographs, 6, 1-83. Chipman, R. K., & Fox, K. A. (1966). Factors in pregnancy blocking: Age and reproductive background of females: Numbers of strange males. Journal of Reproductive Fertility, 12, 399-403. Clulow, F. V., Franchetto, E. A., & Langford, P. E. (1982). Pregnancy failure in the redbacked vole, Clethrionomys gapperi. Journal of Mammalogy, 63, 499-500. Hasler, J. F., & Banks, E. M. (1975). Morphological changes in the ovaries and other organs of the collared lemming (Dicrostonyx groenlandicus) during pregnancy and pseudopregnancy. Canadian Journal of Zoology, 53, 12-18. Heske, E. J., & Nelson, R. J. (1984). Pregnancy interruption in Microtus ochrogaster: Laboratory artifact or field phenomenon? Biology of Reproduction, 31, 97-103. Huck, U. W., Bracken, A. C., & Lisk, R. D. (1983). Female-induced pregnancy block in the golden hamster. Behavioral and Neural Biology, 38, 190-193. Labov, J. B. (1981). Pregnancy blocking in rodents: Adaptive advantages for females. The American Naturalist, 118, 361-371. Mallory, F. F., & Brooks, R. J. (1980). Infanticide and pregnancy failure: Reproductive strategies in the female collared lemming (Dicrostonyx groenlandicus). Biology of Reproduction, 22, 192-196. Schwagmeyer, P. L. (1979). The Bruce effect: An evaluation of male/female advantages. The American Naturalist, 114, 932-938. Yamazaki, K., Beauchamp, G. K., Wysocki, C. J., Bard, J., Thomas, L., & Boyse, E. A. (1983). Recognition of H-2 types in relation to the blocking of pregnancy in mice. Science (Washington, D.C.), 221, 186-188.
BEHAVIORAL AND NEURAL BIOLOGY 4 4 , 4 8 5 - 4 9 1
BRIEF REPORT Failure of Strange Females to Cause Pregnancy Block in Collared Lemmings, Dicrostonyxgroenlandicus RONALD J.
BROOKS, MELODY
A.
DONALD, AND LIN SCHWARZKOPF1
Department of Zoology, University of Guelph, Guelph, Ontario N1G 2W1, Canada The effects of exposure to unfamiliar females on pregnancy success of recently mated females were examined in collared lemmings (Dicrostonyx groenlandicus). Four days after mating, females in their home cage were exposed to strange, female intruders that were either nonpregnant or 16 days pregnant. Other recently mated females were introduced to the home cage of 16-day-pregnant females. Pregnancy success of the recently mated females was not reduced in any of these treatments. In the paired encounters, there was no relationship between dominance status and pregnancy status, nor between dominance and pregnancy success. These results do not support the hypothesis that in species in which females are aggressive and readily commit infanticide, unfamiliar females should cause other females to terminate early-stage pregnancies. © 1985AcademicPress, Inc.
Although pregnancy block by strange males was discovered more than 20 years ago and has been demonstrated in many species of rodents (Labov, 1981; Schwagmeyer, 1979), there is still no widely accepted explanation of its selective value to the aborting female (Heske & Nelson, 1984; Schwagmeyer, 1979). Recently, however, some authors have proposed that pregnancy failure is an adaptive response of females to infanticidal behavior of strange males (Huck, Bracken, & Lisk, 1983; Labov, 1981; Mallory & Brooks, 1980). Thus, when a newly pregnant female encounters a strange male who is likely to kill her neonates, she should terminate the pregnancy and remate with the new male, because the new male is unlikely to kill his own offspring (Labov, 1981 ; Mallory & Brooks, 1980). This tactic confers a selective advantage because the cost to the female of termination, committed investment, and time is small for unimplanted embryos compared to loss of neonates. Recently, Huck et al. (1983) attempted to test this hypothesis using 1 Financial support was provided by NSERC Grant A5990 to R. J. Brooks. Send requests for reprints to Dr. Brooks. 485 0163-1047/85 $3.00 Copyright © 1985 by Academic Press, Inc. All rights of reproduction in any form reserved.
486
BROOKS, DONALD, AND SCHWARZKOPF
golden hamsters (Mesocricetus auratus). They reasoned that because female hamsters are more aggressive than males and because they readily kill unrelated, undefended neonates, these females should be able to terminate pregnancy in other females as readily as males do in other rodents. They found that pregnancy success was significantly reduced among recently mated females when they were defeated in encounters with other pregnant females.. In collared lemmings, Dicrostonyx groenlandicus, as in golden hamsters, females readily commit infanticide (Mallory & Brooks, 1980), and are highly aggressive (Brooks & Banks, 1973), especially toward other females. Therefore, we tested the hypothesis of Huck et al. (1983) that in such species females would abort preimplantation pregnancies when confronted by unfamiliar females. Experimental subjects were derived from lemmings trapped at Churchill, Manitoba in 1980 and 1981. They were maintained on an 18.5 L:5.5 D photoperiod at 18 + 4°C and were housed individually in opaque plastic cages (44 x 28 x 15 cm) with corn grit substrate and paper towels for nesting. Guinea pig chow (Ralston Purina) and water were provided ad libitum. Estrous, nulliparous females were paired with males and if ejaculation was observed within 30 min, females were left with the males for 24 hr, after which the male was removed. Implantation in collared lemmings occurs on Day 5 postcoitum (Hasler & Banks, 1975). All experimental females were tested 4 days after mating and are referred to as "recentlymated" females. Experiment 1. Because even fairly mild external stressors and disturbance may block pregnancy in collared lemmings (Mallory & Brooks, 1980), we tried to separate effects of such trauma from effects of the presence of strange females per se. In the first experiment, we tested whether pregnancy success of females in their home cage would be reduced when they were exposed to the odor or physical presence of a strange female. Thirty-six recently mated females were assigned randomly to one of three treatments or to a control. In Treatment 1, 200 cc of feces and soiled cage substrate from a strange, nonpregnant female and a paper towel soaked with fresh urine from the same female were introduced to the home cage of a recently mated female. In Treatment 2, a sexually mature, nonpregnant, nonlactating female, previously housed in another room, was introduced into the home cage of the experimental female. Frequency of attack, bite, mount, tooth chatter, and initiation of boxing was recorded for 15 min. Behavioral acts were defined as in Brooks and Banks (1973). The intruder female was removed after 24 hr. In Treatment 3, a 16-daypregnant female was introduced into the home cage of a recently mated female. Behavior was recorded as in Treatment 2. Intruders were removed after 4 hr to reduce mortality. In a control treatment, clean substrate
P R E G N A N C Y SUCCESS IN LEMMINGS
487
and a paper towel were added to the home cage of a recently mated female. The purpose of Treatments 2 and 3 was to expose experimental females to relatively unaggressive (nonpregnant) females and to females in late gestation that we expected to be more aggressive than the recently mated experimental females (Huck et al., 1983). Experiment 2. In this experiment, we tested the hypothesis that females would terminate pregnancy when they encountered an aggressive, strange female in the latter's home area. Nineteen recently mated females were assigned randomly to a treatment and a control. In Treatment 1, recently mated females were introduced into a 16-day-pregnant female's home cage. Behavior was recorded for 15 min as in Experiment 1, after which the recently mated females were removed immediately to prevent serious injury and returned to their home cage. In the control, recently mated females were picked up and placed in a clean unoccupied cage and returned to their home cage after 15 min. Following all treatments, females were left in their home cages for the remainder of gestation. At parturition, date of birth and litter size were recorded. In all experiments, if the 16day-pregnant female failed to give birth, we did not use the data involving that female as we could not be certain she was pregnant at the time of the encounter. In Experiment 1, there was no significant difference between the number of females having litters in the control versus the other three treatments (X2(3) = 1 . 5 5 , p > .05). Similarly, mean litter sizes among treatments were the same [ANOVA F(3, 27) = 0.834, p > .05 (Table 1)]. In T r e a t m e n t 2, recently mated resident females attacked and bit nonpregnant intruders more often than the intruders attacked and bit residents, but there were no differences between the two groups in frequency of o c c u r r e n c e of the remaining behavior patterns measured (Table 2). There was great variation in behavioral response during the encounters. F o r example, 3 of 10 intruder females died during or shortly after the encounters, whereas in 2 of 10 pairings none of the five measured behavior patterns occurred. In T r e a t m e n t 3, recently mated resident females were more likely to bite than were 16-day-pregnant intruders (Table 2). There were no significant differences between these two groups in any of the other measured patterns of behavior. H o w e v e r , some females were badly injured in both groups. In E x p e r i m e n t 2, there was no significant difference in pregnancy rate between treatment and control groups [Xz(1) = 0.114, p > .05 (Table 1)]. No significant differences occurred between 16-day-pregnant (home cage) and recently mated females in frequency of any measured behavior patterns (Table 2). Recently mated females that subsequently had a litter attacked 16-daypregnant females in the latter's home cage 39.0 +_ 24.1 (mean + SD)
488
BROOKS, DONALD, AND SCHWARZKOPF
TABLE 1 Number of Successful Pregnancies and Mean Litter Size (± SD) in Each Treatment Group in Experiments 1 and 2 Sample size
Number of successful pregnancies
Mean litter size
Treatment 1 Recently mated female and soiled cage substrate
10
8
3.0 + 1.5
Treatment 2 Recently mated female and nonpregnant female
10
7
3.6 -4- 2.9
6
6
2.2 --- 0.8
10
9
3.2 --- 0.8
9
6
3.0 _+ 1.6
10
7
3.0 ± 2.1
Group Experiment 1
Treatment 3 Recently mated female (home cage) and 16-day-pregnant female Control Recently mated female and clean bedding Experiment 2
Treatment 1 16-Day-pregnant female (home cage) and recently mated female Control Recently mated female into strange cage
t i m e s p e r e n c o u n t e r (n = 6). T h o s e t h a t s u b s e q u e n t l y f a i l e d to h a v e a l i t t e r a t t a c k e d 64.7 ___ 22.5 t i m e s p e r e n c o u n t e r (n = 3). This d i f f e r e n c e w a s n o t significant (t(7) = 1.36, p > .05). I n b o t h i n s t a n c e s , r e c e n t l y mated intruders attacked more often than did their 16-day-pregnant resident o p p o n e n t s (21.5 _+ 16.7 a n d 51.0 --_ 22.1 a t t a c k s , r e s p e c t i v e l y , f o r t h e latter). H o w e v e r , neither o f these differences was significant (when r e c e n t l y m a t e d f e m a l e s d e l i v e r e d a litter; t(5) = 1.26, p > .05; w h e n r e c e n t l y m a t e d f e m a l e s d i d n o t d e l i v e r a litter, t(2) = 0.549, p > .05). T h e r e f o r e , t h e r e w a s n o t e n d e n c y f o r s u b o r d i n a t e b e h a v i o r in r e c e n t l y m a t e d f e m a l e s to b e a s s o c i a t e d w i t h p r e g n a n c y failure, n o r w a s t h e r e a n y t e n d e n c y f o r
PREGNANCY SUCCESS IN LEMMINGS
489
,-.t
g +1 +1 +1 ÷1 +1 0 e~
A
+1 +1 +1 ÷1 +1 ©
0
o+ i
o
.~
+1 +1 ÷1 ÷1 +1
.3
~,~ v
~ve ÷1 +1 ÷1 +1 41
d ~ d d 0
÷1
~+.' ~2 .+~1 2 +'
o+
÷1 +1 ÷1 +1 +1 e~
. ~ o
490
BROOKS, DONALD, AND SCHWARZKOPF
females in advanced stages of pregnancy to dominate recently mated females. Recently mated female lemmings terminate pregnancy when exposed to strange males or even to repeated gentle handling (Mallory & Brooks, 1980). Furthermore, female rodents abort more readily when younger (e.g., Chipman & Fox, 1966) and when nulliparous (Clulow, Franchetto, & Langford, 1982), and our recently mated females were young and nulliparous. In addition, females apparently can cause other females to block in hamsters (Huck et al., 1983) and in mice (Yamazaki, Beauchamp, Wysocki, Bard, Thomas, & Boyse, 1983). Nevertheless, our results indicated that neither odor nor presence of strange females in the home cage or in an unfamiliar cage terminate preimplantation pregnancy in collared lemmings. As expected, recently mated (usually pregnant) females were aggressive, and usually defeated nonpregnant intruders. However, no clear dominance emerged between recently mated and 16-day-pregnant females, although the former bit more often when in their home cage. Therefore, our results do not support the hypothesis that in rodents in which females are aggressive and likely to commit infanticide, females should also be able to induce abortion in other females. This result would also appear not to support the hypothesis that potential infanticide is a selective force that makes pregnancy block adaptive for a female confronted by a novel conspecific. However, even if female lemmings did terminate pregnancy after encountering a strange female, as hamsters apparently do (Huck et al., 1983), this would not constitute strong support for this hypothesis. Females may avoid infanticide when confronted by a strange male by terminating pregnancy and remating with the strange male. In contrast, females that terminate pregnancy when confronted by a strange female will gain nothing. They can probably remate because males are usually available (Brooks & Banks, 1973), but even if they do remate, the new litter may still be susceptible to the intruder female. Hence, while the hypothesis is logical for male intruders (Labov, 1981; Mallory & Brooks, 1980), it is not for female intruders (Huck et al., 1983). We suggest that the results of Huck et al. (1983) may be explained more parsimoniously as the result of physical trauma suffered by subordinate females. In lemmings, this trauma was apparently insufficient to terminate pregnancy. In fact, recently mated females tended to be more aggressive than 16-day-pregnant females, but even when they "lost" in the experimental encounter, two out of three still gave birth. In addition, although it did not emerge clearly in our study, in nature, female lemmings at their homesites are likely to dominate intruders of either sex (Brooks & Banks, 1973). This is probably true for most rodents. Females on homesites are unlikely to terminate pregnancy because of losing a conflict. Pregnancy termination in response even to strange males has been
PREGNANCY SUCCESS IN LEMMINGS
491
documented only in the laboratory. Perhaps future consideration of its selective value should involve a serious attempt to integrate laboratory work on chemosensory recognition (Yamazaki et al., 1983) with some pertinent field data on population structure and density (Heske & Nelson, 1984). At present, such data are lacking. REFERENCES Brooks, R. J., & Banks, E. M. (1973). Behavioural biology of the collared lemming Dicrostonyx groenlandicus (Traill): An analysis of acoustic communication. Animal Behaviour Monographs, 6, 1-83. Chipman, R. K., & Fox, K. A. (1966). Factors in pregnancy blocking: Age and reproductive background of females: Numbers of strange males. Journal of Reproductive Fertility, 12, 399-403. Clulow, F. V., Franchetto, E. A., & Langford, P. E. (1982). Pregnancy failure in the redbacked vole, Clethrionomys gapperi. Journal of Mammalogy, 63, 499-500. Hasler, J. F., & Banks, E. M. (1975). Morphological changes in the ovaries and other organs of the collared lemming (Dicrostonyx groenlandicus) during pregnancy and pseudopregnancy. Canadian Journal of Zoology, 53, 12-18. Heske, E. J., & Nelson, R. J. (1984). Pregnancy interruption in Microtus ochrogaster: Laboratory artifact or field phenomenon? Biology of Reproduction, 31, 97-103. Huck, U. W., Bracken, A. C., & Lisk, R. D. (1983). Female-induced pregnancy block in the golden hamster. Behavioral and Neural Biology, 38, 190-193. Labov, J. B. (1981). Pregnancy blocking in rodents: Adaptive advantages for females. The American Naturalist, 118, 361-371. Mallory, F. F., & Brooks, R. J. (1980). Infanticide and pregnancy failure: Reproductive strategies in the female collared lemming (Dicrostonyx groenlandicus). Biology of Reproduction, 22, 192-196. Schwagmeyer, P. L. (1979). The Bruce effect: An evaluation of male/female advantages. The American Naturalist, 114, 932-938. Yamazaki, K., Beauchamp, G. K., Wysocki, C. J., Bard, J., Thomas, L., & Boyse, E. A. (1983). Recognition of H-2 types in relation to the blocking of pregnancy in mice. Science (Washington, D.C.), 221, 186-188.