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Environmental features determining successful rearing in the mutant mouse Staggerer
Physiology & Behavior, Vol. 32, pp. 225-228. Copyright ©PergamonPress Ltd., 1984. Printedin the U.S.A.
0031-8384/84$3.00 + .00
Environmental Features Determining Successful Rearing in the Mutant Mouse Staggerer J.-M. G U A S T A V I N O
Laboratoire d'Ethologie et Sociobiologie, Equipe de R e c h e r c h e Associt;e au C . N . R . S . No. 885, Universit6 Paris XIII, A v e n u e J.-B. Clrment 93430, Villetaneuse, France R e c e i v e d 27 J a n u a r y 1983 GUASTAVINO, J.-M. Environmentalfeatures determining successful rearing in the mutant mouse staggerer. PHYSIOL BEHAV 32(2) 225-228, 1984.--The mutant mouse staggerer is unable to rear her pups to weaning unless special precautions are taken. The following environmental conditions were found to contribute to compensate for the maternal behavioral deficits of the staggerer: (1) the foster pups used in a constrainingbox to stimulate the lactating staggerer mother are 4 days old. (2) The mother is enforced to stay in close physical contact with these pups for at least 12 hours immediately after delivery. (3) The staggerer pups are transferred to a normal lactating mother to suckle her for the first 12 hours of life.
Staggerer mutant mouse
Maternal behavior
Suckling
THE mutant staggerer mouse spontaneously appeared in the Jackson Memorial Laboratory and was described for the first time by Sidman, Lane and Dickie [8]. The mutation is dependant upon one recessive gene, which determines the development of the cerebellum. The mutant is maintained by crossing heterozygous animals since females homozygous for the staggerer gene are unable to rear their pups to adulthood under standard laboratory conditions. Thus most pups die at birth choked by the amniotic membrane which the mother is unable to remove. Surviving pups are dispersed in the cage, and when trying to suck the mother they are rejected. Ignored by the mother, they usually die of cold or hunger. We have recently demonstrated that, by altering the standard laboratory environment of the staggerer mother, she may be able to rear about 2/3 of her litter until weaning [5]. At delivery, the experimenter opens the amniotic membrane, cleans the pups and transfers them to a normal female to suckle her for the first 24 hours. The mutant mother, in turn, receives the 4-day-old pups of the normal foster mother. To prevent the staggerer mother from escaping the pups she is placed with them in a small box. Enforced to stay in close vicinity of the pups, she gives up her resistance and allows the pups to suckle her. This communication reports a series of experiments that were undertaken to evaluate some of the parameters that were effective in compensating for the behavioral deficits of the staggerer mother. Three experiments were performed. In the first experiment, we studied the role of the age of the foster pups, assuming that older pups provide more suckling
Environmental compensation
stimulation than younger ones. In a second experiment, the importance of the length of constraint was studied systematically. Focussing on the litter rather than the mother, a third experiment was undertaken in which we investigated the role of nursing by a normal mother during the first 24 hours of life of the staggerer pups. GENERAL METHOD
Animals The animals used in this study were mutant mice of the C57BL/6 strain. Females were sg/sg and males sg/+. This strain and type of mutant have been reared in our laboratory under special conditions [4] since 1977. Parents were provided by the "Institut Pasteur." They lived in 35x 35x 20 cm standard cages with a 12 hour photoperiod of darkness and 12 hour of lightness, under constant temperature (24°), and with free access to solid and soft food and to water. All the females were nulliparous and were used only once. Intercrossing sg/sg females with sg/+ males, we obtained a total of 133 litters. In Experiment 1, we used 21, in Experiment 2, 29 and in Experiment 3, 83 litters. One week before delivery, the pregnant females were placed in single cages, 10x 20x 10 cm.
Apparatus The box used for constraining the staggerer mother with her pups was cylindrical, 9 cm in diameter and 5 cm high. The floor was made of fine-meshed cloth, which easily
~The research for this article was partially supported by the DGRST (Grant No. 78-3080).
225
226 formed a cavity under the weight of the animals, the pups staying at the bottom and the mother above. Holes in the cover of the box permitted air circulation and the distribution of water, and food [5].
GUASTAVINO
100--
Measures and Statistics Group differences were analysed by the X" test on the basis of surviving pups (N.S., p>0.02). E X P E R I M E N T 1: V A R I A T I O N O F T H E A G E O F T H E F O S T E R P U P S
Ca.
Method The mother was constrained with the pups in two successive stages. Stage 1: Immediately after delivery, the mutant's pups were removed and the mother was forced to stay with 6 foster pups in the box for 24 hours. Stage 2: Following the initial 24 hour period of fostering, the foster pups were removed and her own litter, which in the meantime had been tended by a normal female, were housed in a small 10x 10 cm cage. The small size of the cage helped the staggerer pups to find their mother. The dimension of the cage was increased to 10x 20 cm at day 15 at which age the pups were able to return to the nest without help. The litters used in this experiment were divided into two groups according to the age of the foster pups which were given to the staggerer mother during the 24-hour of constraint. (1) l-day-old pups group. The pups were aged 0-24 hours and were called " l - d a y pups." Twelve litters were used. (2) 4-day-old pups group. The pups were aged 3-4 days and were called "4-day pups." Nine litters were used.
Results and Discussion Figure i shows the percentage of surviving pups according to the age of the pups fostered during the period of environmental constraint. Fostering of 4-day old pups resulted in survival of 67 percent of her own litter at 21 days of age. Fostering of 1-day old pups resulted in survival of only 6.8 percent of her own litter at 21 days. Differences between these two groups were significant at p<0.01. Four-day-old pups have a greater suckling experience, need more food, and are more likely to empty the mammary glands. They may therefore be more effective in stimulating milk production than 1-day-old pups. The importance of emptying the mammary gland has been stressed by several authors [2, 6, 7]. Fuchs and Wagner [3] demonstrated that the rate of oxytoxin release in the mother rabbit increased with the age of the pups. Furthermore, Blass and Teicher [1] showed that newborn rat pups fail to attach to the teats unless they had been coated by amniotic fluid and/or saliva from the mother or the pups. The staggerer mother is unable to lick her own teats and can therefore not provide the pups with necessary guidance to her nipples. Experienced 4-day-01d pups manage to find the nipples without guidance. Older pups coat the nipples with saliva, thereby facilitating attachment for the staggerer litters when the pups are returned to their biological mother after the first 24 hours of mothering by foster mothers.
".
........ i
Part.r6tJon
3
6
, ........... [] ..................... 112
,,.,
[] i
21
I
days
FIG. 1. Shows the percentage of individual pups surviving as a function of the age of the foster pups, from birth to weaning. [].--D...E]..-E] 1 day; l i - I B - B - I I 4 days.
duration of the constraint. The litters used in this study were assigned to the following groups, according to the length of constraint:
Groups
Length of Constraint
Number of Litters
Long Constraint Medium Constraint Short Constraint
12 hours 6 hours 1-3 hours
16 7 6
Results and Discussion As shown in Fig. 2, 2.7 percent of the Short constraint group, and 6 percent of the Medium constraint group survived at least to weaning. In the Long constraint group, 67 percent survived at least to weaning. The upper curve in Fig. 2 shows the survival of the group constrained for 24 hours as in Experiment I. The survival rate of this group compared to Long constraint group did not significantly differ at day 21 (p >0.05) suggesting that 12 hours of constraint is adequate to attain a nearly maximal survival rate. The present results suggest that there is a minimal time during which the mother must be constrained with the pups in order for milk production to occur. The differences at day 3 between Medium constraint and Short constraint groups in survival rate may be due to the longer fostering time in the Medium constraint group. It appears from these data that the period necessary for suckling to develop is about 12 hours because constraint for a longer period did not further improve the chance of survival until weaning. E X P E R I M E N T 3: V A R I A T I O N O F C A R E G I V E N TO T H E L I T T E R
E X P E R I M E N T 2: V A R I A T I O N O F T H E L E N G T H O F T H E P E R I O D OF CONSTRAINT
Method The same procedure for constraining the mother with 4-day old pups was used as in Experiment l, except for the
To evaluate the importance of the care given to the staggerer"s litter while fostered by the normal mother, we compared the survival rate of litters which had been fostered by a normal mother, with litters that had been reared exclusively by the staggerer.
E N V I R O N M E N T AND M A T E R N A L BEHAVIOR
227 cent of the Non-fostered pups survived compared to 36 percent of the Fostered pups. The relatively high survival rate in the Fostered pups at day 3 may be attributed to the good care provided them by a normal mother during their first 24 hours of life. However, even in this group very few pups survived more than 12 days, indicating that the care given by the foster mother was still insufficient and did not fully compensate for the deficient care provided by the staggerer mother. No attempt was made to extend the length of constraint beyond 24 hours. Longer constraint would mean a longer stay for the staggerer litter with the foster mother, which, in turn, would result a greater influence produced by the care of the foster mother.
i Parturition
6
211
days
FIG. 2. Shows the percentage of individual pups surviving as a function of age and constraint duration. 24 hours m - m - B ; 12 hours O - O - O ; 6 hours A - A - A ; 1-3 hours 0 - 0 - 0 .
lO0.
so,
i,
, P
rut
ti
3
• .........
,
.................
6
, 12
..................................
T
A,
;
21
days
FIG. 3. Shows the percentage of individual pups surviving as a function of age and dam type during the first 24 hours. A • . . ~ • •. A remain with own mother; & - A - A adopted by a normal mother.
Method The animals used in this experiment were divided into two groups, Fostered (8 litters) and Non-fostered (75 litters). In the Fostered group, staggerer mother's pups were w i t h drawn immediately after delivery and replaced by an equal number of l-day old foster pups. The staggerer mother and her foster pups were housed in a standard cage and no attempt was made to constrain the mother with the foster pups. After 24 hours, the mother's own pups were returned to her, in the mean time having been cared for by a normal mother. In the Non-fostered group, the pups were reared continuously by their own mutant mother in a standard cage.
Results and Discussion As indicated by Fig. 3, a clear group difference was found in the survival rate (significant at p<0.01). At Day 3, I per-
GENERAL DISCUSSION The inability of the staggerer mother to bring her offspring to adulthood under standard laboratory conditions is an expression of a severe neurological deficit caused by the mutant gene. The present results show that the deficiencies in the maternal behavior of the staggerer can to a large extent be compensated for, by environmental changes that facilitate the initiation of suckling by the pups. This was accomplished by modifying the standard rearing conditions during the first 24 hours in two ways: by constraining the mother with pups within a small area and by replacing her own newborn pups with older foster pups, which already have suckling experience. To rear pups to adulthood, the staggerer mother needs support in two ways. Firstly, she needs pups which can provide sufficient stimulation in terms of intensity and duration to induce milk secretion and milk ejection. Secondly, she needs pups which are able to survive for some time without maternal care. There are several reasons why older pups might be more suitable than younger ones to induce suckling. The importance of experience and of marking nipples with saliva are two factors which were discussed. Moreover older pups are stronger, need more food and presumably are more persistent in their attempts to get access to the teats [9]. In addition, older pups do not seem to be killed by the mother as easily as younger pups, as was reported for hamsters [10]. T h e results of the second experiment demonstrate the importance of the length of time during which the foster pups are constrained with the staggerer mother. One can distinguish between two successive phases in the period of constraint: a first phase, when the staggerer mother still is able to defend herself against solicitation of the pups, and a second phase when the staggerer finally accepts the pups. According to our observations the duration of the first phase is 3-6 hours. A duration of 6-9 hours for the second phase may be adequate because the survival rate showed little difference after 12 and 24 hours of total length of constraint. A small difference in survival rate was observed between the 3-and 6-hour groups which is probably related to the different length of time the pups were fostered by the normal mother. The slight difference found in the effects of suckling between 12 and 24 hours (Experiment 2) suggests that an optimal level of stimulation was reached after 12 hours. The somewhat higher survival rate obtained by stimulation during a longer time, 24 hours, might be due to the fact that the pups had not been cared for by a normal mother for this period. This suggestion is supported by the third experiment
228
GUASTAVINO
w h i c h s h o w e d that care p r o v i d e d b y a n o r m a l m o t h e r d u r i n g a 24-hour p e r i o d is e n o u g h to allow a b o u t o n e t h i r d o f the s t a g g e r e r pups to s u r v i v e until the third day. A l t h o u g h the p r o c e d u r e s d e s c r i b e d a b o v e c o n s i d e r a b l y i m p r o v e d the s u r v i v a l rate o f the s t a g g e r e r s ' litters, 1/3 o f the litters still died d u e to failing m a t e r n a l care. T h e s t a g g e r e r d o e s n o t lick the p u p s , d o e s not build a n e s t a n d n e v e r ret r i e v e s the pups. W h e n s u c k l e d , the s t a g g e r e r m o t h e r ass u m e s a p e c u l i a r position, m o s t o f the time lying o n the side, w h i c h limits a c c e s s o f t h e pups to h e r teats. T h e specific
i m p o r t a n c e of t h e s e v a r i o u s factors is not k n o w n , b u t they m a y all c o n t r i b u t e to explain t h e failure o f t h e s t a g g e r e r to r e a r more t h a n 2/3 of h e r pups e v e n u n d e r c o n s i d e r a b l y improved environmental conditions.
ACKNOWLEDGEMENT The author gratefully acknowledges the assistance of Dr. Larsson and Dr. Goodall with the writing, of Denise Abehassera with the typing and of the ESF with a short term fellowship.
REFERENCES 1. Blass, E. M. and M. H. Teicher. Suckling. Science 210: 15-21, 1980. 2. Caruolo, E. V. Exogenous oxytocin and lactation in the mouse. J Dairy Sei 54: 1207-1211, 1971. 3. Fuch~, A. R. and G. Wagner. Quantitative aspects of release of oxytocin by suckling in unaesthetized rabbits. Aeta Endocrinol (Copenh) 44: 581-592, 1963. 4. Guastavino, J.-M. Sur le drveloppement comportemental de la souris atteinte par la mutation staggerer. C R Seanees Acad Sei (!!!) 286: 137-139, 1978. 5. Guastavino, J.-M. Constraint of the mother with pups restores some aspects of the maternal behavior of the mutant mouse staggerer. Physiol Behav 30: 771-774, 1983.
6. Martinet, J. and L.-M. Houdebine. La lactation. La Recherche 131: 13, 300-310, 1982. 7. Martinet, J., M. Morag and R. Denamur. The role of exogenous oxytocin in lactating ewe. Ann Biol Anita Bioehem Biophys 16: 833-849, 1976. 8. Sidman, R. L., P. W. Lane and M. M. Dickie. Staggerer: a new mutation in the mouse affecting the cerebellum. Science 137: 610-612, 1962. 9. Stoloff, M. L., J. T. Kenny, E. M. Blass and W. G. Hall. The role of experience in suckling maintenance in albino rats. J Comp Physiol Psychol 94: 847-856, 1980. 10. Swanson, L. J. and C. S. Campbell. Induction of maternal behavior in nulliparous golden hamsters (Mesocricetus Auratus). Behav Neural Biol 26: 364--371, 1979.
0031-8384/84$3.00 + .00
Environmental Features Determining Successful Rearing in the Mutant Mouse Staggerer J.-M. G U A S T A V I N O
Laboratoire d'Ethologie et Sociobiologie, Equipe de R e c h e r c h e Associt;e au C . N . R . S . No. 885, Universit6 Paris XIII, A v e n u e J.-B. Clrment 93430, Villetaneuse, France R e c e i v e d 27 J a n u a r y 1983 GUASTAVINO, J.-M. Environmentalfeatures determining successful rearing in the mutant mouse staggerer. PHYSIOL BEHAV 32(2) 225-228, 1984.--The mutant mouse staggerer is unable to rear her pups to weaning unless special precautions are taken. The following environmental conditions were found to contribute to compensate for the maternal behavioral deficits of the staggerer: (1) the foster pups used in a constrainingbox to stimulate the lactating staggerer mother are 4 days old. (2) The mother is enforced to stay in close physical contact with these pups for at least 12 hours immediately after delivery. (3) The staggerer pups are transferred to a normal lactating mother to suckle her for the first 12 hours of life.
Staggerer mutant mouse
Maternal behavior
Suckling
THE mutant staggerer mouse spontaneously appeared in the Jackson Memorial Laboratory and was described for the first time by Sidman, Lane and Dickie [8]. The mutation is dependant upon one recessive gene, which determines the development of the cerebellum. The mutant is maintained by crossing heterozygous animals since females homozygous for the staggerer gene are unable to rear their pups to adulthood under standard laboratory conditions. Thus most pups die at birth choked by the amniotic membrane which the mother is unable to remove. Surviving pups are dispersed in the cage, and when trying to suck the mother they are rejected. Ignored by the mother, they usually die of cold or hunger. We have recently demonstrated that, by altering the standard laboratory environment of the staggerer mother, she may be able to rear about 2/3 of her litter until weaning [5]. At delivery, the experimenter opens the amniotic membrane, cleans the pups and transfers them to a normal female to suckle her for the first 24 hours. The mutant mother, in turn, receives the 4-day-old pups of the normal foster mother. To prevent the staggerer mother from escaping the pups she is placed with them in a small box. Enforced to stay in close vicinity of the pups, she gives up her resistance and allows the pups to suckle her. This communication reports a series of experiments that were undertaken to evaluate some of the parameters that were effective in compensating for the behavioral deficits of the staggerer mother. Three experiments were performed. In the first experiment, we studied the role of the age of the foster pups, assuming that older pups provide more suckling
Environmental compensation
stimulation than younger ones. In a second experiment, the importance of the length of constraint was studied systematically. Focussing on the litter rather than the mother, a third experiment was undertaken in which we investigated the role of nursing by a normal mother during the first 24 hours of life of the staggerer pups. GENERAL METHOD
Animals The animals used in this study were mutant mice of the C57BL/6 strain. Females were sg/sg and males sg/+. This strain and type of mutant have been reared in our laboratory under special conditions [4] since 1977. Parents were provided by the "Institut Pasteur." They lived in 35x 35x 20 cm standard cages with a 12 hour photoperiod of darkness and 12 hour of lightness, under constant temperature (24°), and with free access to solid and soft food and to water. All the females were nulliparous and were used only once. Intercrossing sg/sg females with sg/+ males, we obtained a total of 133 litters. In Experiment 1, we used 21, in Experiment 2, 29 and in Experiment 3, 83 litters. One week before delivery, the pregnant females were placed in single cages, 10x 20x 10 cm.
Apparatus The box used for constraining the staggerer mother with her pups was cylindrical, 9 cm in diameter and 5 cm high. The floor was made of fine-meshed cloth, which easily
~The research for this article was partially supported by the DGRST (Grant No. 78-3080).
225
226 formed a cavity under the weight of the animals, the pups staying at the bottom and the mother above. Holes in the cover of the box permitted air circulation and the distribution of water, and food [5].
GUASTAVINO
100--
Measures and Statistics Group differences were analysed by the X" test on the basis of surviving pups (N.S., p>0.02). E X P E R I M E N T 1: V A R I A T I O N O F T H E A G E O F T H E F O S T E R P U P S
Ca.
Method The mother was constrained with the pups in two successive stages. Stage 1: Immediately after delivery, the mutant's pups were removed and the mother was forced to stay with 6 foster pups in the box for 24 hours. Stage 2: Following the initial 24 hour period of fostering, the foster pups were removed and her own litter, which in the meantime had been tended by a normal female, were housed in a small 10x 10 cm cage. The small size of the cage helped the staggerer pups to find their mother. The dimension of the cage was increased to 10x 20 cm at day 15 at which age the pups were able to return to the nest without help. The litters used in this experiment were divided into two groups according to the age of the foster pups which were given to the staggerer mother during the 24-hour of constraint. (1) l-day-old pups group. The pups were aged 0-24 hours and were called " l - d a y pups." Twelve litters were used. (2) 4-day-old pups group. The pups were aged 3-4 days and were called "4-day pups." Nine litters were used.
Results and Discussion Figure i shows the percentage of surviving pups according to the age of the pups fostered during the period of environmental constraint. Fostering of 4-day old pups resulted in survival of 67 percent of her own litter at 21 days of age. Fostering of 1-day old pups resulted in survival of only 6.8 percent of her own litter at 21 days. Differences between these two groups were significant at p<0.01. Four-day-old pups have a greater suckling experience, need more food, and are more likely to empty the mammary glands. They may therefore be more effective in stimulating milk production than 1-day-old pups. The importance of emptying the mammary gland has been stressed by several authors [2, 6, 7]. Fuchs and Wagner [3] demonstrated that the rate of oxytoxin release in the mother rabbit increased with the age of the pups. Furthermore, Blass and Teicher [1] showed that newborn rat pups fail to attach to the teats unless they had been coated by amniotic fluid and/or saliva from the mother or the pups. The staggerer mother is unable to lick her own teats and can therefore not provide the pups with necessary guidance to her nipples. Experienced 4-day-01d pups manage to find the nipples without guidance. Older pups coat the nipples with saliva, thereby facilitating attachment for the staggerer litters when the pups are returned to their biological mother after the first 24 hours of mothering by foster mothers.
".
........ i
Part.r6tJon
3
6
, ........... [] ..................... 112
,,.,
[] i
21
I
days
FIG. 1. Shows the percentage of individual pups surviving as a function of the age of the foster pups, from birth to weaning. [].--D...E]..-E] 1 day; l i - I B - B - I I 4 days.
duration of the constraint. The litters used in this study were assigned to the following groups, according to the length of constraint:
Groups
Length of Constraint
Number of Litters
Long Constraint Medium Constraint Short Constraint
12 hours 6 hours 1-3 hours
16 7 6
Results and Discussion As shown in Fig. 2, 2.7 percent of the Short constraint group, and 6 percent of the Medium constraint group survived at least to weaning. In the Long constraint group, 67 percent survived at least to weaning. The upper curve in Fig. 2 shows the survival of the group constrained for 24 hours as in Experiment I. The survival rate of this group compared to Long constraint group did not significantly differ at day 21 (p >0.05) suggesting that 12 hours of constraint is adequate to attain a nearly maximal survival rate. The present results suggest that there is a minimal time during which the mother must be constrained with the pups in order for milk production to occur. The differences at day 3 between Medium constraint and Short constraint groups in survival rate may be due to the longer fostering time in the Medium constraint group. It appears from these data that the period necessary for suckling to develop is about 12 hours because constraint for a longer period did not further improve the chance of survival until weaning. E X P E R I M E N T 3: V A R I A T I O N O F C A R E G I V E N TO T H E L I T T E R
E X P E R I M E N T 2: V A R I A T I O N O F T H E L E N G T H O F T H E P E R I O D OF CONSTRAINT
Method The same procedure for constraining the mother with 4-day old pups was used as in Experiment l, except for the
To evaluate the importance of the care given to the staggerer"s litter while fostered by the normal mother, we compared the survival rate of litters which had been fostered by a normal mother, with litters that had been reared exclusively by the staggerer.
E N V I R O N M E N T AND M A T E R N A L BEHAVIOR
227 cent of the Non-fostered pups survived compared to 36 percent of the Fostered pups. The relatively high survival rate in the Fostered pups at day 3 may be attributed to the good care provided them by a normal mother during their first 24 hours of life. However, even in this group very few pups survived more than 12 days, indicating that the care given by the foster mother was still insufficient and did not fully compensate for the deficient care provided by the staggerer mother. No attempt was made to extend the length of constraint beyond 24 hours. Longer constraint would mean a longer stay for the staggerer litter with the foster mother, which, in turn, would result a greater influence produced by the care of the foster mother.
i Parturition
6
211
days
FIG. 2. Shows the percentage of individual pups surviving as a function of age and constraint duration. 24 hours m - m - B ; 12 hours O - O - O ; 6 hours A - A - A ; 1-3 hours 0 - 0 - 0 .
lO0.
so,
i,
, P
rut
ti
3
• .........
,
.................
6
, 12
..................................
T
A,
;
21
days
FIG. 3. Shows the percentage of individual pups surviving as a function of age and dam type during the first 24 hours. A • . . ~ • •. A remain with own mother; & - A - A adopted by a normal mother.
Method The animals used in this experiment were divided into two groups, Fostered (8 litters) and Non-fostered (75 litters). In the Fostered group, staggerer mother's pups were w i t h drawn immediately after delivery and replaced by an equal number of l-day old foster pups. The staggerer mother and her foster pups were housed in a standard cage and no attempt was made to constrain the mother with the foster pups. After 24 hours, the mother's own pups were returned to her, in the mean time having been cared for by a normal mother. In the Non-fostered group, the pups were reared continuously by their own mutant mother in a standard cage.
Results and Discussion As indicated by Fig. 3, a clear group difference was found in the survival rate (significant at p<0.01). At Day 3, I per-
GENERAL DISCUSSION The inability of the staggerer mother to bring her offspring to adulthood under standard laboratory conditions is an expression of a severe neurological deficit caused by the mutant gene. The present results show that the deficiencies in the maternal behavior of the staggerer can to a large extent be compensated for, by environmental changes that facilitate the initiation of suckling by the pups. This was accomplished by modifying the standard rearing conditions during the first 24 hours in two ways: by constraining the mother with pups within a small area and by replacing her own newborn pups with older foster pups, which already have suckling experience. To rear pups to adulthood, the staggerer mother needs support in two ways. Firstly, she needs pups which can provide sufficient stimulation in terms of intensity and duration to induce milk secretion and milk ejection. Secondly, she needs pups which are able to survive for some time without maternal care. There are several reasons why older pups might be more suitable than younger ones to induce suckling. The importance of experience and of marking nipples with saliva are two factors which were discussed. Moreover older pups are stronger, need more food and presumably are more persistent in their attempts to get access to the teats [9]. In addition, older pups do not seem to be killed by the mother as easily as younger pups, as was reported for hamsters [10]. T h e results of the second experiment demonstrate the importance of the length of time during which the foster pups are constrained with the staggerer mother. One can distinguish between two successive phases in the period of constraint: a first phase, when the staggerer mother still is able to defend herself against solicitation of the pups, and a second phase when the staggerer finally accepts the pups. According to our observations the duration of the first phase is 3-6 hours. A duration of 6-9 hours for the second phase may be adequate because the survival rate showed little difference after 12 and 24 hours of total length of constraint. A small difference in survival rate was observed between the 3-and 6-hour groups which is probably related to the different length of time the pups were fostered by the normal mother. The slight difference found in the effects of suckling between 12 and 24 hours (Experiment 2) suggests that an optimal level of stimulation was reached after 12 hours. The somewhat higher survival rate obtained by stimulation during a longer time, 24 hours, might be due to the fact that the pups had not been cared for by a normal mother for this period. This suggestion is supported by the third experiment
228
GUASTAVINO
w h i c h s h o w e d that care p r o v i d e d b y a n o r m a l m o t h e r d u r i n g a 24-hour p e r i o d is e n o u g h to allow a b o u t o n e t h i r d o f the s t a g g e r e r pups to s u r v i v e until the third day. A l t h o u g h the p r o c e d u r e s d e s c r i b e d a b o v e c o n s i d e r a b l y i m p r o v e d the s u r v i v a l rate o f the s t a g g e r e r s ' litters, 1/3 o f the litters still died d u e to failing m a t e r n a l care. T h e s t a g g e r e r d o e s n o t lick the p u p s , d o e s not build a n e s t a n d n e v e r ret r i e v e s the pups. W h e n s u c k l e d , the s t a g g e r e r m o t h e r ass u m e s a p e c u l i a r position, m o s t o f the time lying o n the side, w h i c h limits a c c e s s o f t h e pups to h e r teats. T h e specific
i m p o r t a n c e of t h e s e v a r i o u s factors is not k n o w n , b u t they m a y all c o n t r i b u t e to explain t h e failure o f t h e s t a g g e r e r to r e a r more t h a n 2/3 of h e r pups e v e n u n d e r c o n s i d e r a b l y improved environmental conditions.
ACKNOWLEDGEMENT The author gratefully acknowledges the assistance of Dr. Larsson and Dr. Goodall with the writing, of Denise Abehassera with the typing and of the ESF with a short term fellowship.
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