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The influence of the male on maternal behaviour in the Mongolian gerbil (Meriones unguiculatus)
Anim.Behav.,1976,2.4,372-375
THE INFLUENCE OF THE MALE ON MATERNAL BEHAVIOUR IN THE MONGOLIAN GERBIL (MERIONES UNGUICULATUS) BY J. K. AHROON* & F. G. FIDURA
Department of Psychology, State University College of New York, Geneseo, New York 14454 Abstract. Multiparous pregnant gerbils (Meriones ungu&ulatus)were housed with or without male mates following parturition. Six of seven litters in the 'male-present' condition were found dead by the third day post partum; these females showed very little maternal behaviour. Six of seven litters in the 'nomale' condition were successfully reared through 9 days of observation; these females showed consistently high rates of maternal behaviour. Cannibalism was rare in both conditions, the majority of pup-deaths resulting from neglect. It appears that the presence of the male disrupts maternal behaviour, resulting in neglect of the pups and pup-mortality. The male's presence may interfere with the effective space, or 'territory', necessary to the female for the display of appropriate maternal behaviour.
Certain behavioural patterns of the Mongolian gerbil (Meriones unguieulatus) are reported to differ from those of several related rodent species. Examples include a faster rate of learning than the rat in situations requiring activity (Lippman, Galosy & Thompson 1970; Lippman & Thompson 1972), use of a sebaceous gland for territorial marking (Thiessen et al. 1970), and high rates of early pup-mortality (Marston & Chang 1965; Norris & Adams 1972b). These mortality rates are much higher than those usually reported for other rodent species, and are not the result of cannibalism, which is extremely rare in the gerbil (Woodcock 1955; Norris & Adams 1972b; Adams & Norris 1973). Pup-mortality appears to be associated with the presence of the male gerbil. Those reports in which the male was either allowed to remain with the female and litter until weaning (Marston & Chang 1965), or was not removed until the second day post partum (Norris & Adams 1972b), find generally higher rates of pup mortality than studies in which the male was removed prior to, or at, parturition (Woodcock t955; Kaplan & Hyland 1972). Since cannibalism is rarely observed, and the male is never reported to harm the pups in any overt way (Marston & Chang 1965; Norris & Adams 1972b), it follows that the observed pup deaths result from a lack of appropriate maternal care on the part of the gerbil mother. The presence of the male may serve to hinder, or completely suppress, the establishment of appropriate maternal behaviour following parturition. The present experiment was designed to determine whether male-presence is a variable *Present address: State University of New York, Binghamton, New York 13901, U.S..A.
influencing pup-mortality in the gerbil, a n d to observe the expression of maternal behaviour in the female gerbil. Methods The subjects were fourteen pregnant multiparous gerbils and their respective mates, obtained from Tumblebrook Farms, Inc., West Brookfield, Massachusetts. Each pair was housed in a clear glass aquarium (60 x 32 x 42 cm), equipped with ad libitum water and Purina lab chow. Standard animal litter was used as cage bedding, and two paper towels per cage were provided for nest material. A 12-hr light-12-hr dark lighting regimen was used, the dark phase being from midnight to noon. A panel of six 150-W outdoor floodlights and six 25-W red lights suspended 91.44 cm over the observation cages provided illumination. Cages were checked daily, and at parturition the number of pups born was recorded. No culling of litters was performed. Treatment Proeednre Seven of the fourteen female subjects were housed with their mates prior to, and during, the experimental observation period ('male-present' condition). For the remaining seven subjects, the males were removed at parturition ('no-male' condition). The observations were performed in replicates, with four female subjects under observation at any one time.
Observation Procedure A system of BRS timers and counters, and a push-button keyboard, were used in recording the following four categories of maternal behaviour: (a) sniffing/licking: touching and licking of a pups' head and body; (b) retrieving: 372
AHROON: & FIDURA: MALE INFLUENCE ON GERBIL MATERNAL BEI-IAVIOUR carrying a pup back to nest area; (c) nursing: body arched over pups, or laying on one side, exposing nipple area; (d) nest-building: straightening or rearranging of nest material. From day 2 (following parturition on day 0) through day 10, observations were made during four 10-min periods per day, equally spaced over the daily light and dark phase. A behavioural pattern was recorded if exhibited during any 30-s interval of the 10-rain observation period, and frequencies were summed over periods per day. With twenty 30-s intervals in each 10-rain period, multiplied by four periods daily, the maximum frequency for each behavioural category was 80 (20 • 4 = 80). Each subject was assigned a score between 0 and 80 for each behavioural category. A rating of nest quality was made during each observation period. Incidences of cannibalism, usually documented from evidence o f pup remains, were recorded. Pup deaths due to causes other than cannibalism also were recorded. Results The day 2 category scores provided the only available comparison of the groups' scores, due to termination of observations on those subjects that had lost their entire litter starting on day 3. The single most striking finding of the present study was the observation that six of seven litters in the male-present condition failed to survive past day 3. Except for the few that were cannibalized, all pups were found intact, lying dead in their cages, and there was no evidence of wounds indicating attacks. Seventy-two per cent (twenty-four of thirty-three) of the pups in the male-present condition were lost, compared with a 24 per cent (nine o f thirty-seven) loss in the no-male condition (Fig. 1). This difference was statistically reliable (Z2 = 16.3, dr= 1, P < 0-01). The overall mean litter size was 5.0,
373
and the two group means were not significantly different. Male-presence significantly depressed sniffing/licking (F = 7.5; d f = 1, 9; P < 0.05), retrieving (F = 7-76, d f = 1, 9; P < 0.05), and nest-building ( F = 5.73; d f = 1, 9; P < 0.05) behaviour (Fig. 2). No 'male-present' coBdition females built better than a poor quality nest; while the majority of'no-male' condition females built adequate, or good nests. There were no significant differences in frequency of nursing between the two groups. Incidences o f cannibalism (seven of seventy), which occurred only on days 0, 1, and 2, were too low for analysis. Figure 1 demonstrates that the majority of such incidences were found in the male-present group; however, the incidences could not be attributed to either male or female. Daily qualitative observations were taken on all subjects, and males, on days 0 and 1, and during the scheduled observation periods. The majority o f the male-present subjects demonstrated 'frenetic' behaviour, i,e. erratic, almost continual activity, on day 0. During the first half of day 0, three of the seven males pursued their mates, for approximately ten minutes, and several mounts were noted. Female gerbils can experience post p a r t u m oestrus; however, subjeets were not examined for pregnancy, in order to minimize experimenter interference. The initial 'frenetic" level o f female behaviour, with rare pup contact, was maintained until the end of day 3, when six of the seven subjects had lost all their pups. Aggressive encounters between males and females were observed on day 1; however, in six cases the frequency of such encounters decreased by day 2, and the six males remained spatially removed from female and litter. None of these litters survived past SNIFFiNG/L1C4C'NG
NURSING
2O
o=
,•10 ,?.G
~2 ?~o
0
I
2
FA H 3
4
[]
MALE-PRESENT
[]
NO- MALE
[]
CANNIBALISM
. . . . 5
6
.EL.__ 7
RETRIEVING
NEST BUILDING
+1
B
9
F"A_ I0
DAYS POST PARTUM
Fig. 1. Daily pup losses, including cannibalism, for male-present (N = 33) and no-male (N = 37) conditions.
__--.7,~:z:z
Fig. 2. Mean frequency scores for behavioural measures on day 2, based on the total score, over four observation periods, for the behaviour.
374
ANIMAL
BEHAVIOUK,
day 3. Upon removal, the majority of dead pups showed no evidence of stomach distension, or whitish coloration, suggesting that they had not received any milk. One male-female pair displayed frequent and consistent aggressive encounters, which increased over the first few days post partum. By day 3, a dominance hierarchy appeared established, and the male was consistently found in the same area as the female and litter. This litter was successfully maintained through the 9-day period. While females in the no-male condition also demonstrated a 'frenetic' level initially, it dissipated rapidly, and the frequency of maternal behaviour increased daily. One subject in the no-male condition never demonstrated any maternal behaviour and alternated between 'frenetic' activity and 'freezing', in which she remained crouched on all four feet, motionless, for as long as 20 rain at a time. This female's litter was found dead on day 1. Initiation of maternal behaviour, i.e. recurrent incidences during each observation period, was shown on day 1 in the no-male group, contrary to Kaplan & Hyland (1972) who reported that no consistent maternal behaviour was observed before day 2. Frequency of all maternal behaviour except nursing declined in the no-male group by day 8. Non-pup-related activity increased, somewhat, on day 10. Discussion
The rresent results indicate that the presence o f the male depresses the frequencies of sniffing/ licking, retrieving and nest-building in the female gerbil. A continual 'frenetic' level of activity, largely precluding pup contact, was also shown by the females housed with their mates following parturition. The extreme variability of nursing behaviour, both within and between subjects, may account for the lack of a significant depression effect on this measure. Pup-mortality was clearly and significantly higher in the presence of the male. The work o f Rosenblatt (1969) with rats suggests that the first few days following parturition are critical because disruption of developing maternal responsiveness at this time appears to prevent its later expression. Adams & Norris (1973) suggest that the presence of the male gerbil may represent such a disturbance. Nyby, Thiessen & Wallace (1970) report that both male and female gerbils seek out and defend territory by means of dominance encounters, and that some area o f space may be important for adaptive functioning
24,
2
in the gerbil (Thiessen 1968; Thiessen et al. 1970; Thiessen, Owen & Lindzey 1971). In addition, the female is also reported to demonstrate greatly increased marking behaviour and aggression following parturition (Thiessen 1973). A proposed explanation for the findings of the present study is that the female gerbil, being territorial, may demand some increase in territorial space following birth of a litter, a change necessary for the development of appropriate maternal behaviour. If a new dominance relationship is not established following this shift, the male's presence in the territory may represent a disruptive influence. Such an interference in spatial demands would serve to hinder or depress the expression of maternal behaviour during the first critical days. Aggressive encounters between males and females were observed on day 1. In the six unsuccessful pairs, the frequency of aggressive encounters subsequently decreased, and males removed themselves from physical contact with female and litter. No dominance hierarchy was apparent. The re-establishment of a territorial relationship, post partum, would appear to be related to the expression of appropriate maternal behaviour in the female gerbil. REFERENCES
Adams, C. S. & Norris, M. L. (1973). Observations on reproduction in the Mongolian gerbil, Meriones unguiculatus. J. Reprod. & Fert., 33, 185-188. Kaplan, H. & Hyland, S. (1972). Behavioural development in the Mongolian gerbil. Anim. Behav., 20, 147-154. Lippman, L. G., Galosy, R. A. & Thompson, R. W. (1970). Passive avoidance learning in gerbils and rats. J. comp. physioL PsychoL, 73, 269-273. Lippman, L. G. & Thompson, R. W. (1972). Exploration and activity in the gerbil and the rat. Paper presented at the annual meeting of the Midwestern Psychological Association, Cleveland, May. Marston, J. & Chang, M. (1965). The breeding, management and reproductive physiology of the Mongolian gerbil (Meriones unguiculatus). Lab. Anim. Care, 15, 34--48. Norris, M. L. & Adams, C. E. (1972). Mortality from birth to weaningin the Mongolian gerbil (Meriones unguiculatus). Lab. Anita., 6, 49-53. Nyby, J., Thiessen, D. D. & Wallace, P. (1970). Social inhibition of territorial marking in the Mongolian gerbil (Meriones unguiculatus). Psychon. Sci., 21, 310-312. Rosenblatt, J. (1969). The development of maternal responsiveness in the rat. Am. J. Orthopsychiat., 39, 36-56. Thiessen, D. D. (1968). The roots of territorial marking in the Mongolian gerbil: A problem of speciescommon topography. Behav. Res. Meth. & lnstru., 1, 70--76.
AI-IROON & FIDURA: MALE INFLUENCE ON GERBIL MATERNAL BEHAVIOUR Thiessen, D. D. (1973). Footholds for survival. Am. Scientist, 61, 346--351. Thiessen, D. D., Lindzey, G., Blum, S. L. & Wallace, P. (1970). Social interactions and scent marking in the Mongolian gerbil (Meriones unguiculatus). Anim. Behav., 19, 505-513. Thiessen, D. D., Owen, K. & Lindzey, G. (1971). Mechanism of territorial marking in the male
375
and female Mongolian gerbil (Mgriones unguiculatus). J. comp. physioL PsychoL, 77, 38-47. Woodcock, W. H. (1955). Management and breeding of a new laboratory species, Meriones libyeus. Anita. Techns. Ass., 6, 10-14.
(Received 12 September 1974; revived 2 April 1975; MS. number: M619)
THE INFLUENCE OF THE MALE ON MATERNAL BEHAVIOUR IN THE MONGOLIAN GERBIL (MERIONES UNGUICULATUS) BY J. K. AHROON* & F. G. FIDURA
Department of Psychology, State University College of New York, Geneseo, New York 14454 Abstract. Multiparous pregnant gerbils (Meriones ungu&ulatus)were housed with or without male mates following parturition. Six of seven litters in the 'male-present' condition were found dead by the third day post partum; these females showed very little maternal behaviour. Six of seven litters in the 'nomale' condition were successfully reared through 9 days of observation; these females showed consistently high rates of maternal behaviour. Cannibalism was rare in both conditions, the majority of pup-deaths resulting from neglect. It appears that the presence of the male disrupts maternal behaviour, resulting in neglect of the pups and pup-mortality. The male's presence may interfere with the effective space, or 'territory', necessary to the female for the display of appropriate maternal behaviour.
Certain behavioural patterns of the Mongolian gerbil (Meriones unguieulatus) are reported to differ from those of several related rodent species. Examples include a faster rate of learning than the rat in situations requiring activity (Lippman, Galosy & Thompson 1970; Lippman & Thompson 1972), use of a sebaceous gland for territorial marking (Thiessen et al. 1970), and high rates of early pup-mortality (Marston & Chang 1965; Norris & Adams 1972b). These mortality rates are much higher than those usually reported for other rodent species, and are not the result of cannibalism, which is extremely rare in the gerbil (Woodcock 1955; Norris & Adams 1972b; Adams & Norris 1973). Pup-mortality appears to be associated with the presence of the male gerbil. Those reports in which the male was either allowed to remain with the female and litter until weaning (Marston & Chang 1965), or was not removed until the second day post partum (Norris & Adams 1972b), find generally higher rates of pup mortality than studies in which the male was removed prior to, or at, parturition (Woodcock t955; Kaplan & Hyland 1972). Since cannibalism is rarely observed, and the male is never reported to harm the pups in any overt way (Marston & Chang 1965; Norris & Adams 1972b), it follows that the observed pup deaths result from a lack of appropriate maternal care on the part of the gerbil mother. The presence of the male may serve to hinder, or completely suppress, the establishment of appropriate maternal behaviour following parturition. The present experiment was designed to determine whether male-presence is a variable *Present address: State University of New York, Binghamton, New York 13901, U.S..A.
influencing pup-mortality in the gerbil, a n d to observe the expression of maternal behaviour in the female gerbil. Methods The subjects were fourteen pregnant multiparous gerbils and their respective mates, obtained from Tumblebrook Farms, Inc., West Brookfield, Massachusetts. Each pair was housed in a clear glass aquarium (60 x 32 x 42 cm), equipped with ad libitum water and Purina lab chow. Standard animal litter was used as cage bedding, and two paper towels per cage were provided for nest material. A 12-hr light-12-hr dark lighting regimen was used, the dark phase being from midnight to noon. A panel of six 150-W outdoor floodlights and six 25-W red lights suspended 91.44 cm over the observation cages provided illumination. Cages were checked daily, and at parturition the number of pups born was recorded. No culling of litters was performed. Treatment Proeednre Seven of the fourteen female subjects were housed with their mates prior to, and during, the experimental observation period ('male-present' condition). For the remaining seven subjects, the males were removed at parturition ('no-male' condition). The observations were performed in replicates, with four female subjects under observation at any one time.
Observation Procedure A system of BRS timers and counters, and a push-button keyboard, were used in recording the following four categories of maternal behaviour: (a) sniffing/licking: touching and licking of a pups' head and body; (b) retrieving: 372
AHROON: & FIDURA: MALE INFLUENCE ON GERBIL MATERNAL BEI-IAVIOUR carrying a pup back to nest area; (c) nursing: body arched over pups, or laying on one side, exposing nipple area; (d) nest-building: straightening or rearranging of nest material. From day 2 (following parturition on day 0) through day 10, observations were made during four 10-min periods per day, equally spaced over the daily light and dark phase. A behavioural pattern was recorded if exhibited during any 30-s interval of the 10-rain observation period, and frequencies were summed over periods per day. With twenty 30-s intervals in each 10-rain period, multiplied by four periods daily, the maximum frequency for each behavioural category was 80 (20 • 4 = 80). Each subject was assigned a score between 0 and 80 for each behavioural category. A rating of nest quality was made during each observation period. Incidences of cannibalism, usually documented from evidence o f pup remains, were recorded. Pup deaths due to causes other than cannibalism also were recorded. Results The day 2 category scores provided the only available comparison of the groups' scores, due to termination of observations on those subjects that had lost their entire litter starting on day 3. The single most striking finding of the present study was the observation that six of seven litters in the male-present condition failed to survive past day 3. Except for the few that were cannibalized, all pups were found intact, lying dead in their cages, and there was no evidence of wounds indicating attacks. Seventy-two per cent (twenty-four of thirty-three) of the pups in the male-present condition were lost, compared with a 24 per cent (nine o f thirty-seven) loss in the no-male condition (Fig. 1). This difference was statistically reliable (Z2 = 16.3, dr= 1, P < 0-01). The overall mean litter size was 5.0,
373
and the two group means were not significantly different. Male-presence significantly depressed sniffing/licking (F = 7.5; d f = 1, 9; P < 0.05), retrieving (F = 7-76, d f = 1, 9; P < 0.05), and nest-building ( F = 5.73; d f = 1, 9; P < 0.05) behaviour (Fig. 2). No 'male-present' coBdition females built better than a poor quality nest; while the majority of'no-male' condition females built adequate, or good nests. There were no significant differences in frequency of nursing between the two groups. Incidences o f cannibalism (seven of seventy), which occurred only on days 0, 1, and 2, were too low for analysis. Figure 1 demonstrates that the majority of such incidences were found in the male-present group; however, the incidences could not be attributed to either male or female. Daily qualitative observations were taken on all subjects, and males, on days 0 and 1, and during the scheduled observation periods. The majority o f the male-present subjects demonstrated 'frenetic' behaviour, i,e. erratic, almost continual activity, on day 0. During the first half of day 0, three of the seven males pursued their mates, for approximately ten minutes, and several mounts were noted. Female gerbils can experience post p a r t u m oestrus; however, subjeets were not examined for pregnancy, in order to minimize experimenter interference. The initial 'frenetic" level o f female behaviour, with rare pup contact, was maintained until the end of day 3, when six of the seven subjects had lost all their pups. Aggressive encounters between males and females were observed on day 1; however, in six cases the frequency of such encounters decreased by day 2, and the six males remained spatially removed from female and litter. None of these litters survived past SNIFFiNG/L1C4C'NG
NURSING
2O
o=
,•10 ,?.G
~2 ?~o
0
I
2
FA H 3
4
[]
MALE-PRESENT
[]
NO- MALE
[]
CANNIBALISM
. . . . 5
6
.EL.__ 7
RETRIEVING
NEST BUILDING
+1
B
9
F"A_ I0
DAYS POST PARTUM
Fig. 1. Daily pup losses, including cannibalism, for male-present (N = 33) and no-male (N = 37) conditions.
__--.7,~:z:z
Fig. 2. Mean frequency scores for behavioural measures on day 2, based on the total score, over four observation periods, for the behaviour.
374
ANIMAL
BEHAVIOUK,
day 3. Upon removal, the majority of dead pups showed no evidence of stomach distension, or whitish coloration, suggesting that they had not received any milk. One male-female pair displayed frequent and consistent aggressive encounters, which increased over the first few days post partum. By day 3, a dominance hierarchy appeared established, and the male was consistently found in the same area as the female and litter. This litter was successfully maintained through the 9-day period. While females in the no-male condition also demonstrated a 'frenetic' level initially, it dissipated rapidly, and the frequency of maternal behaviour increased daily. One subject in the no-male condition never demonstrated any maternal behaviour and alternated between 'frenetic' activity and 'freezing', in which she remained crouched on all four feet, motionless, for as long as 20 rain at a time. This female's litter was found dead on day 1. Initiation of maternal behaviour, i.e. recurrent incidences during each observation period, was shown on day 1 in the no-male group, contrary to Kaplan & Hyland (1972) who reported that no consistent maternal behaviour was observed before day 2. Frequency of all maternal behaviour except nursing declined in the no-male group by day 8. Non-pup-related activity increased, somewhat, on day 10. Discussion
The rresent results indicate that the presence o f the male depresses the frequencies of sniffing/ licking, retrieving and nest-building in the female gerbil. A continual 'frenetic' level of activity, largely precluding pup contact, was also shown by the females housed with their mates following parturition. The extreme variability of nursing behaviour, both within and between subjects, may account for the lack of a significant depression effect on this measure. Pup-mortality was clearly and significantly higher in the presence of the male. The work o f Rosenblatt (1969) with rats suggests that the first few days following parturition are critical because disruption of developing maternal responsiveness at this time appears to prevent its later expression. Adams & Norris (1973) suggest that the presence of the male gerbil may represent such a disturbance. Nyby, Thiessen & Wallace (1970) report that both male and female gerbils seek out and defend territory by means of dominance encounters, and that some area o f space may be important for adaptive functioning
24,
2
in the gerbil (Thiessen 1968; Thiessen et al. 1970; Thiessen, Owen & Lindzey 1971). In addition, the female is also reported to demonstrate greatly increased marking behaviour and aggression following parturition (Thiessen 1973). A proposed explanation for the findings of the present study is that the female gerbil, being territorial, may demand some increase in territorial space following birth of a litter, a change necessary for the development of appropriate maternal behaviour. If a new dominance relationship is not established following this shift, the male's presence in the territory may represent a disruptive influence. Such an interference in spatial demands would serve to hinder or depress the expression of maternal behaviour during the first critical days. Aggressive encounters between males and females were observed on day 1. In the six unsuccessful pairs, the frequency of aggressive encounters subsequently decreased, and males removed themselves from physical contact with female and litter. No dominance hierarchy was apparent. The re-establishment of a territorial relationship, post partum, would appear to be related to the expression of appropriate maternal behaviour in the female gerbil. REFERENCES
Adams, C. S. & Norris, M. L. (1973). Observations on reproduction in the Mongolian gerbil, Meriones unguiculatus. J. Reprod. & Fert., 33, 185-188. Kaplan, H. & Hyland, S. (1972). Behavioural development in the Mongolian gerbil. Anim. Behav., 20, 147-154. Lippman, L. G., Galosy, R. A. & Thompson, R. W. (1970). Passive avoidance learning in gerbils and rats. J. comp. physioL PsychoL, 73, 269-273. Lippman, L. G. & Thompson, R. W. (1972). Exploration and activity in the gerbil and the rat. Paper presented at the annual meeting of the Midwestern Psychological Association, Cleveland, May. Marston, J. & Chang, M. (1965). The breeding, management and reproductive physiology of the Mongolian gerbil (Meriones unguiculatus). Lab. Anim. Care, 15, 34--48. Norris, M. L. & Adams, C. E. (1972). Mortality from birth to weaningin the Mongolian gerbil (Meriones unguiculatus). Lab. Anita., 6, 49-53. Nyby, J., Thiessen, D. D. & Wallace, P. (1970). Social inhibition of territorial marking in the Mongolian gerbil (Meriones unguiculatus). Psychon. Sci., 21, 310-312. Rosenblatt, J. (1969). The development of maternal responsiveness in the rat. Am. J. Orthopsychiat., 39, 36-56. Thiessen, D. D. (1968). The roots of territorial marking in the Mongolian gerbil: A problem of speciescommon topography. Behav. Res. Meth. & lnstru., 1, 70--76.
AI-IROON & FIDURA: MALE INFLUENCE ON GERBIL MATERNAL BEHAVIOUR Thiessen, D. D. (1973). Footholds for survival. Am. Scientist, 61, 346--351. Thiessen, D. D., Lindzey, G., Blum, S. L. & Wallace, P. (1970). Social interactions and scent marking in the Mongolian gerbil (Meriones unguiculatus). Anim. Behav., 19, 505-513. Thiessen, D. D., Owen, K. & Lindzey, G. (1971). Mechanism of territorial marking in the male
375
and female Mongolian gerbil (Mgriones unguiculatus). J. comp. physioL PsychoL, 77, 38-47. Woodcock, W. H. (1955). Management and breeding of a new laboratory species, Meriones libyeus. Anita. Techns. Ass., 6, 10-14.
(Received 12 September 1974; revived 2 April 1975; MS. number: M619)