ELSEVIER Applied Animal Behaviour Science 48 (1996) 215-224

APPLIED ANIMAL BEHAVIOUR

SCIENCE

Effects of immediate and early post-partum separation on maintenance of maternal

responsiveness in parturient multiparous goats

A. Rankez a, A. Quiles a, * , M.L. Hevia a, F. Sotillo a, M.C. Rdrez b

a Departamento de Produccicin Animal, Facultud de Veterinaria, Universidad de Murcia, Campus de Espinardo, 30071 Murcia, Spain

b Departamento de Psiquiatriu y Psicologia Social, Facultad de Psicologia, Universidad de Murcia, Campus de Espinardo, 30071 Murciu. Spuin

Accepted 6 December 1995

Abstract

The subject of study consisted of the determination of the effects of separation, either immediate or after brief mother-young post-partum contact, on the maintenance of the maternal response in multiparous goats of Murciano-Granadina breed, having eliminated every visual, olfactory, auditory, or taste stimulus that could be used as a reminder by the mother. Fifty goats and their 82 kids were used in the study. The goats were kept away from their kids for l/2 or 1 h when the separation took place immediately after birth, and for 1, 8, or 24 h when it took place after a brief 5min post-partum contact between mother and young. At the end of the separation both were put together in a stall. The half-hour following the reunion was recorded on video tape. The results have shown that, as for an immediate post-partum separation, the maternal response is maintained (lo/lo) after a separation of l/2 h. However, the response is null (O/ 10) after l-h separations. After a brief mother-young post-partum contact, the results show that there is maternal response after separations of 1 and 8 h (lo/ 10). On the other hand, a separation of 24 h brings about the extinction of that maternal response (lo/lo) and breaks any mother-young ties that may have been established during that brief period of initial contact.

Keywords: Goat; Parental behaviour; Critical period; Maternal-filial bond

* Corresponding author.

016%1591/96/$15.00 0 1996 Elsevier Science B.V. All rights reserved PII SO168-1591(96)01028-3

216 A, Ramirez et al./AppliedAnimal Behaviour Science 48 (1996) 215-224

1. Introduction

In goats, as in other ungulate species, maternal behaviour is strongly associated with the moment of birth, therefore the development of an adequate maternal response depends on the contact that mother and young make in the first post-partum hours. It may also be stated that there is a sensitive period, of a relatively short length depending on the species, during which the maternal response of the female towards its offspring is established (Hersher et al., 1957, Hersher et al., 1958; Alexander, 1960; Bouissou, 1968; Klopfer, 1971; Le Neindre and Garel, 1976). Hersher et al. (1963) define it as a period in which “the sensibility of the mother is highest on facing certain particular stimuli” so that outside that period the probability of the mother accepting its offspring is small.

In the caprine species, Collias (1956) and Klopfer et al. (1964) have found a very short period of maternal sensitivity after parturition (1 h), finding no difference between primiparous and multiparous goats. They also noticed that maternal sensitivity extended after a brief mother-young post-partum contact. In this way, these authors saw offspring acceptance by mothers that remained 5 min with their kids and were later separated for 3 h. However, contrary to what was found by the above-mentioned authors, Lickliter (1982) observed that the length of the period of maternal sensitivity is not so brief in the case of goats with experience (multiparous), while it is in goats without experience. In this author’s study there were acceptances (6/6) for their offspring in multiparous goats which were separated from their kids immediately after birth, and kept away for 2 h. Based on these results, Lickliter (1982) inferred that a brief mother-young post-partum contact to extend maternal sensitivity is not necessary, therefore disagreeing with Collias (1956) and Klopfer et al. (1964).

The discrepancy between these authors has led us to verify, in the first place, whether maternal sensitivity in multiparous goats is as short as Collias (1956) and Klopfer et al. (1964) point out, or significantly longer as Lickliter (1982) does. In the second place, we shall try to prove whether a brief mother-young post-partum contact increases such sensitivity. To do this, we have used a greater number of animals than were used in previous works, and to prevent methodological differences, we have eliminated any possible influence of foetal fluids and membranes.

2. Materials aud methods

2.1. Animals

The study was carried out at EMEGA research station (Estaci6n de Mejora Ganadera) which belongs to the Comunidad Autonoma de Murcia, from August 1992 to March 1993. Fifty multiparous goats (second and third parturition) of Murciano-Granadino breed were used. They were divided into two herds. The goats were inseminated, and in addition a male was present for a month after insemination. This allowed us to predict the date of birth giving. All the parturitions were natural, and the goats were allowed to choose the birth site. The goats were identified with birth collars.

All the animals were kept under the same handling and feeding conditions, although

A. Ramirez et al./Applied Animal Behaviour Science 48 (1996) 215-224 217

the two herds stayed in different barns, which consisted of an indoor pen and an outdoor enclosure. The goats had free access to both places. Feeding took place in the indoor pen with cereal hay ad libitum, supplemented daily with about 500 g of dehydrated alfalfa granules and barley grains.

2.2. Separation

In this study, two types of mother-young separations were done. The first type was done with 20 goats that were separated from their offspring immediately after birth (Group I). Of the 20, te n were separated for 0.5 h and the other ten for 1 h. The second type was done with 30 goats, separated from their kids 5 min after birth (Group II). Of these 30 goats, ten were separated for 1 h, another ten for 8 h and the remaining ten for 24 h. In the case of a single birth, the period of contact between dam and kid began when the mother licked its kid for the first time. In the case of twins, the period began when the mother licked the first-born for the first time. If the second kid of the twin birth was born out of this period of mother-young contact (5 min), it was removed immediately after birth.

Once the kids were separated from their mothers, they were placed in clean towels and carried away from the dam in order to prevent smelling, tasting, or hearing by the dam. The kids were dried and identified with numbered collars and remained in the pen until the moment of reunion. The kids that were separated for 8 and 24 h were bottle-fed with maternal colostrum to provide them with the necessary immunoglobulin to immu- nize and secure their first life hours. Kids were kept under a hot source of protection in winter, Immediately after the birth of all kids, the dams were separated from the herd and put in individual pens in another barn. The foetal fluids were eliminated soon after expulsion to prevent smelling and tasting stimuli. When the isolation period was over, the kids were led to the mother’s barn, and were put in the middle of the dam’s pen.

2.3. Behavioural observation

A video camera (CANON VM-E2) set in an adjacent pen, allowed us to record the first half-hour after dams and kids were reunited.

2.4. Valuation of maternal behaviour

Maternal behaviour was assessed according to the following three criteria.

2.4.1. Acceptance or refusal behaviour The degree of acceptance or refusal has been evaluated according to the following

categories: 1. Acceptance: dams have an immediate interest towards their offspring. The dam licks

the kid and allows it to suck.

218 A, Ram& et al./AppliedAnimal Behaviour Science 48 (1996) 215-224

2. Refusal type I: the dam approaches, smells and even licks the kids before leaving them. Later, the dam approaches the kids but with no contact, and when they try to suck, it shuns and sometimes butts them.

3. Refusal type II: the dam approaches and smells its kids, but does not lick them and leaves them. Later, the dam shuns them when they approach her, and sometimes butts them.

4. Refusal type III: the dam shows no interest towards its kids from the beginning. It shuns or butts them when they approach.

2.4.2. Maternal care (MC) To determine the degree of maternal acceptance we have used two factors: the

distance of separation and whether or not there was maternal care towards the offspring during the half-hour of reunion. We have noted observations every 5 min, making, therefore, six observations per goat. The valuation of the maternal care was as follows: every 5 min, the distance between the dam and the kid was registered (< 1 m, l-3 m, > 3 m); maternal care was determined as care-giving such as licking, or persistent attention towards the kid. The dimensions of the pens were 8 X 4 m.

2.4.3. Activity of mothers The time spent or the number of frequencies done by the dam in the following

behaviour patterns were recorded: ?? Standing: the dam stands up. - Recumbency: the dam lies down. - Licking: the dam licks the kid. - Eating: the mother eats. - Grooming: the dam licks itself. - Attempting: number of approaches towards the kids without reaching them, and

leaving immediately. - Avoiding: number of times the dam shuns the kids when they approach. - Butting: number of times the dam butts the kids when they approach.

2.5. Evaluation of kids’ behaviour

?? Standing: the kid stands up. - Recumbency: the kid lies down. - Sleeping: the kid sleeps.

2.6. Statistical analysis

Comparisons of proportions of non-maternal goats were carried out using a Chi-square test for comparison of the two sample cases. Statistical analysis of all behavioural parameters was carried out using a parametric test (one-way analysis of variance) for between-group comparisons of time and number of actions performed.

A. Ramirez et al./AppliedAnimal Behuviour Science 48 (1996) 215-224 219

3. Results

Duration of mother-young separation had a strong effect on maternal responsiveness in Group I (following separation immediately after birth). All goats with 0.5 h separation accepted their offspring, whereas no goats did so after 1 h (Table 1, X2 = 20, d.f. = 1, P < O.OOl>. The latter refusal included some of each type. Duration of mother-young separation had a less important effect on the maternal responsiveness in Group II (following separation after 5 min of post-partum contact). All goats with 1 and S-h separation periods accepted their offspring, whereas no goats did so after 24 h (Table 1, X2 = 20, d.f. = 1, P < 0.001). In the latter only two types of refusal were found.

Degree of maternal care (indicated by distance between dam and kid and presence or absence of maternal care, Table 21, is higher in goats separated immediately after birth for 0.5 h than in those separated for 1 h. In the same way, goats separated for 1 and 8 h after remaining 5 min after birth with their offspring also showed a higher maternal response than those separated for 24 h.

Results of Table 3 (effects of after birth mother-young separations on activities by mothers during the first half-hour of reunion) showed that type (immediate or after 5 min of contact) and mother-young separation period significantly modified the time spent by mothers in almost all the activities observed. Only in grooming were no significant differences observed in the different types of separations. Goats separated for 1 h immediately after birth and those separated for 24 h, after 5 min of post-partum contact, did not lick their offspring. On the contrary goats from other types of separation did (49 d.f., F = 48.4, P < 0.001). In the same way, goats separated for 1 h immediately after birth and those separated for 24 h, after 5 min of post-partum contact, performed other activities not done by the goats of the other separation types (eating: 49 d.f., F = 58.0, P < 0.001; approaching: 49 d.f., F = 4.4, P < 0.01; shunning: 49 d.f., F = 25.2, P < 0.001; butting: 49 d.f., F = 9.0, P < 0.001). Significant differences were also found in the time goats spent standing or lying (49 d.f., F = 48.4, P < 0.001). Differences between separation types are specified in Table 3.

The behaviour of kids was modified by the type and duration of the mother-young separation. Significant differences were found in four of the five separation types with

Table 1 Comparison of maternal behaviour after different periods of separation between mothers separated immedi- ately after partmition (n = 20) and those that remained 5 min with their offspring (n = 30)

Herd

I I II II II

Separation

Immediate-O.5 h Immediate- 1 h After 5 min- 1 h After 5 min-8 h After 5 min-24 h

Acceptance

lO/lO o/10

IO/10 IO/10 O/IO

Refusal

Type I

O/IO 2/10 O/IO o/10 o/10

Type II

O/IO 3/10 o/10 o/10 S/IO

Type III

O/IO 5/10 O/IO o/10 2/10

220 A. Ramirez et al./Applied Animal Behuviour Science 48 (1996) 215-224

Table 2 Degree of maternal care, indicated by distance between dam and kid and presence (+) or absence (-) of maternal care. Six observations (one every 5 mitt) were made on each of ten mother/young pairs in each group, so figures are out of 60 observations

Separation Distance between dam and kid

<lm 1-3m >3m

+ - + - + -

Immediate-O.5 h Immediate- 1 h After 5 mm- 1 h

After 5 mm-8 h After 5 min-24 h

60 _ _

- 5 1 1 53 60 -

60 3 51

Table 3 Effects of after birth mother-young separations on activities by mothers during the first half hour of reunion. One way analysis of variance for between-group comparisons (mean SD)

Immediate After 5 min F P

1/2h lh lh 8h 24h

Standing (mitt) 30.0 f 0.0 a 22.7f 1.5 b 30.0 f 0.0 a 30.0 * 0.0 a 18.4f0.9’ 48.4 * * * Recumbency (mitt) O.OfO.O a 7.3* 1.5 b 0.0 f 0.0 B o.o*o.o a 11.7*0.9s 48.4 ?? t ??

Licking kid (min) 15.6rt0.6 a 0.0 f 0.0 b 13.5f 1.3 c 13.7 + 0.8 ac 0.0f0.0b 48.4 ?? * * Grooming (mitt) 0.2fO.l 0.1 fO.l o.o+o.o 0.1 fO.l 0.1 *0.1 1.7 - Eating (mitt) O.OfO.O a 1.0*0.2 b o.o*o.o a O.OfO.O a 4.650.5’ 58.0 * * * Approaching (n) O.OfO.O a 0.8 f 0.4 ab 0.0 f 0.0 a 0.0 f 0.0 a 1.0*0.4b 4.4 * ??Shunning (n) O.OfO.O a 2.1*0.5 b o.o*o.o a 0.0 + 0.0 a 2.4&0.3 b 25.2 ’ * * Butting ( n) O.OfO.O a 1.1 *0.4 b 0.0 f 0.0 a O.OfO.O a 1.8f0.5b 9.0 ***

?? ? ? P <O.Ol; ***P<o.OOl. Different letters mean that there are significant differences between the different times of separation.

respect to the time in which the kids remained standing or lying (Table 4, 81 d.f., F = 135.9, P < 0.001). In the same way, the kids separated for 1 h immediately after birth and those separated for 24 h, after 5 min post-partum contact, slept significantly longer than those from the other separation types (49 d.f., F = 48.4, P < 0.001).

Table 4 Effects of after birth mother-young separations on activities by kids during the first half-hour reunion. One way analysis of variance for between-group comparisons (mean SD)

Immediate After 5 mm F P

1/2h, rr= 16 1 h, n= 16 lh,n=16 8h, n= 17 24h, n= 17

Standing (mitt) 29.9rtO.l a 14.7*o.g b 29.1 +0.9 a’ 28.5+0.5’ 18.4*0.5 d 135.9 * * * Recumbency (mm) 0.1*0.1 a 15.3kO.S b 0.9 f 0.9 ac 1.5*o.5c 11.5f0.5d 135.9 *** Sleeping (mitt) 0.0 f 0.0 a 9.6f0.7 b 0.5 + 0.5 a o.o*o.o a 8.1f0.5b 113.6 ?? **

*** P<O.ool. Different letters mean that there are significant differences between groups.

A. Rumirez et al. /Applied Animul Behuoiour Science 48 (1996) 215-224 221

4. Discussion

Our results clearly prove that there is a sensitive period after birth giving in the domestic goat. But, these results, that clearly show a very quick diminution of maternal sensibility after parturition, are different from those of Lickliter (1982), who observed in multiparous goats acceptance of kids after 2-h separations. It is true, though, that our results support the theory of Klopfer et al. (1964) who denoted that goats that had no contact with their new-boms during the hour after parturition suffered a sudden decrease in maternal sensibility. Gubemick (1980) obtained similar results when he studied maternal ‘imprinting’ or maternal ‘labelling’. This author noticed that two mothers, which had no post-partum contact with their offspring, refused both their own and alien kids when the acceptance-refusal test was done, 1 h after birth. On the other hand, our results show that five mothers separated immediately for 1 h and eight mothers separated after 5 min for 24 h showed some initial and brief curiosity towards their kids. Our experience suggests that this was only a research behaviour towards the new companion sharing their habitat.

The difference between the results of Lickliter (1982) and ours with regard to the duration of the sensitive period in multiparous goats made us propound the hypothesis that there were differences in breed and that there might even be individual differences. On the other hand, we came to think that the elimination of the foetal membranes and fluids might have had a decisive influence in these results. This question we think should be looked into in later works. Despite this variability, we have the clear fact that the immediate separation after parturition of mother and offspring during a small period causes clear disturbances, sometimes irredeemable for the formation of maternal-filial bonds.

It had been studied as well in animals of other species: Hudson and Mullord (1977) and Le Neindre and D’Hour (1988) in the bovine species or Smith et al. (1966) and Poindron and Le Neindre (1980) in the ovine species. In observing these works, we noticed that the period of maternal sensitivity in goats is shorter than those found in cows and sheep. In this manner, acceptances took place in cows after several hours of separation after birth (Hudson and Mullord, 1977 and Le Neindre and D’Hour, 1988). In sheep, Smith et al. (1966) observed acceptances after separations of 8 h after parturition. Likewise, Poindron and Le Neindre (1980) noticed a sudden decline of maternal interest in experiment sheep towards their offspring after 12-h separations. This interest was null after 24-h separations. We can conclude, after all these theories, that goats have a shorter sensitive period than cows and sheep, because while in goats this period lasts between l/2 and 2 h, in cows it can last 5 h and in sheep a maximum of 12 h.

With a brief maternal-filial contact the period of maternal sensitivity will be extended. This fact had already been tested by Hudson and Mullord (1977) in the bovine species, and their results were very similar to ours because these authors observed acceptance of the calf by those cows that had a period of separation of under 12 h, after a small initial post-partum contact. These authors observed though that 24-h separations brought about maternal refusal. Our study shows that a 5min post-partum contact between mother and offspring brings about an extension of that sensitivity and that the mother is receptive at least 8 h after birth. However, this capability of acceptance of the

222 A. Ramirer et al./Applied Animal Behuviour Science 48 (1996) 215-224

offspring by the mothers is found completely extinguished after 24-h separations. In the species studied by us, Klopfer et al. (1964) observed how primiparous goats that had little maternal-filial post-partum contact with their kids and that were separated for 1, 2, and 3-h periods had totally accepted their kids. This agrees with our results in multiparous goats, but it may be advisable to analyse it in following studies, when maternal sensibility ends in primiparous goats. Nevertheless, Lickliter (1982) pointed out that a brief post-partum maternal-filial contact was not necessary for a later manifestation of maternal sensibility. Our results show that such manifestations may be found only after very brief separations (under 1 h), unless the great influence of foetal fluids is established in later works as was pointed out by L&y and Poindron (1987) in the ovine species, or unless there is a great variability among races or even among individuals. However, our work has clearly shown that a brief post-partum contact between mother and offspring is fundamental to extend maternal sensibility in time.

Gubemick et al. (1979) and Gubemick (1980) studied the existence or lack of imprinting in the caprine species. The goats had a 5-min post-partum contact with their offspring. They were then separated and reunited 1 h later for the acceptance-rejection test. Results showed that 13/21 goats accepted both their own and alien kids. Three out of 21 accepted only their own kids and 3/21 mothers rejected both their own and alien kids. Two out of 21 goats rejected their own but accepted alien ones. These results back our own in the sense that a 5-min post-partum contact increases maternal receptivity (18/21 goats accepted their own or alien kids vs 2/2 mothers that rejected both their own and alien kids after an immediate post-partum separation). Furthermore, results obtained by Gubemick et al. (1979) and Gubemick (1980) suggested that mothers did not select their own kids, and therefore that maternal ‘imprinting’ in goats might not occur as rapidly as previously reported (Klopfer et al., 1964). Moreover, Gubemick (1980) found that neither age alone nor behaviour of the alien kids was the major factor in acceptance or rejection since alien kids not in contact with their own mother were accepted by other mothers whether the kids were anaesthetized (thus eliminating behaviour) or were older (2 days old) and awake. Yet alien kids in contact with their own mother were rejected under both conditions. In a later work, Gubemick (Gubemick, 1981a, Gubemick, 1981b) tried to fix the mechanisms of maternal ‘labelling’ in goats. The results showed that maternal labelling in goats appears to be based upon cues passed from the mother to her kid by licking and through mother’s milk. These cues could act alone or in combination allowing mothers to identify their own and refuse alien kids.

Contrary to Gubemick (Gubemick, 1980, Gubemick, 1981a, Gubemick, 198 lb), Romeyer and Poindron (1992) pointed out goats’ ability to show selective care for their kids after post-partum mother-young contact ranging from 2.5 to 12 h (mean: 5.0 h). In this study, 18/19 mothers were found to be selective and to reject alien young presented to them and the rejection was independent of the age of the alien (range: 3 to 28 h, mean 9.3 h) and of duration of mother-young contact prior to the test. The difference of results with respect to those of Gubemick (Gubemick, 1980, Gubemick, 1981 a, Guber- nick, 1981b) is explained in the time of mother-kid exposure prior to separation. So, whereas a very short exposure (5 min), followed by a long period of isolation before testing was used in Gubemick studies, Romeyer and Poindron used a longer duration of

A. Ramirez et al./Applied Animal Behaviour Science 48 (1996) 215-224 223

exposure (average 5 h) followed by a short isolation session. Nevertheless, from results obtained by Romeyer and Poindron, it appears that the dynamics of establishment of exclusive bonding in goats was not slower than those observed in sheep and the difference observed so far rests in the major role played by labelling in goats, whereas in sheep this process seemed to play a limited role in exclusive bonding based upon individual olfactory signatures (Poindron et al., 1988; Alexander et al., 1989; Poindron and L.&y, 1990; L&y et al., 1991; Porter et al., 1991).

Finally, from our results we clearly see that maternal acceptance or rejection will completely modify the behaviour of the offspring. In those cases where there is acceptance, it will bring about an adequate onset of the typical behavioural patterns of the newborn (nursing attempts, nursing, activities, etc.), and, in those cases where there is maternal rejection, it will bring about an abolishment of those typical patterns.

5. Conclusions

Our results corroborate the fact that there is a sensitive period in the domestic goat, this period lasting under 1 h for multiparous goats of Murciano-Granadina breed. Also, a brief maternal-filial contact after parturition extends maternal sensibility, at least 8 h after birth giving, even though this sensibility does extinguish after separations of 24 h.

Acknowledgements

We wish to thank all the people who made this study possible by their participation in the statistical analysis: M.J. Madrid and A. Pelegrin, as well as the staff of the Estacion de Mejora Ganadera of Murcia. We are grateful to I. Veisser for her comments on the manuscript.

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