Establishment of the mother-lamb bond

The link between the ewe and the lamb is displayed immediately lambing. Maternal behavior is induced by endocrine changes that occur in ewes during the peripartum period, mainly the decrease in the progesterone (P4) concentration and the increase on estrogen and oxytocin concentrations^11,12. In response to these changes, and only in this period, the ewe is strongly attracted to the amniotic fluid that surrounds the lamb¹³. Cleaning of the lamb during the first 20 to 30 min helps the mother to recognize her offspring¹⁴. After 60 to 120 min, if the mother receives a different offspring from her own or if she has not previously recognized her lamb, she rejects it¹⁴. The ewe only directs her maternal behavior toward the lambs that were identified as their own offspring during the first postpartum minutes¹⁵. Therefore, to keep the bond it is important that the lamb and the mother can identify each other among other animals in the group. Smell of the offspring is important for the memory of the mother, but the mother also recognizes her lamb through hearing and vision¹⁶.

The first behaviors displayed by the lambs after birth lead to reach the teat and suckle¹³. If the mother accepts her offspring to suckle means that she has recognized it and accepted as her own¹⁷. Lambs also recognizes their mother through sensory mechanisms, primarily hearing and vision¹⁸, which increases the chances of survive¹⁹. During the immediate postpartum period the mother-lamb bond is characterized by a high frequency of suckling and a strong tendency to be in physical proximity during the day^20,21. Although temporary separations of short duration during this period do not have consequences on the later mother-lamb bond¹³, they can generate transient behavior changes in the mother. For example, ewes can move away from their lamb when humans are present²².

Natural weaning

Natural weaning is characterized by the replacement of milk by solid food and the acquisition of social independence of the lamb². During the first 2 wk of the life, ewes allow lambs to suckle every time they require it and gradually, as the lactation proceeds, rejection is more frequent²³. During the period of lactation and the lamb growth, suckling frequency decreases at time that the physical distance between the ewe and lamb increase^20,21. At the same time, the lamb is familiarized and adapted to the consumption of solid food². The decrease of the suckling frequency is also associated with rumen development²⁴. For example, in Santa Inés lambs, rumen development is achieved when lambs reach approximately 15 kg of weight²⁵, allowing the lamb to change the diet.

The production of ewes’ milk is one of the main factors that influence the age of the natural weaning of their lambs²⁶. Age of natural weaning may also vary according to the nutritional status of the ewes; one of the factors that mostly affect is mother’s milk production²⁷. Suckling ends with the weaning of the lamb, about 4 to 5 mo of age²⁶.

Artificial weaning

Artificial weaning is the forced end of suckling, the end of milk supply by the ewes to their lambs, and usually involves physical separation, and therefore the loss of the mother ^2,3,4. Artificial weaning is commonly applied in sheep production systems, since it improves the reproductive and productive results. In meat and wool sheep production, weaning is done to improve body condition and weight, since they influence positively the conception rates, prolificacy and weight of lambs at birth and at weaning^28,29. In sheep milk production systems artificial weaning is done early to obtain more milk, and is associated with the artificial rearing of lambs with dairy substitutes⁽⁴⁾.

Artificial weaning time varies depending on the purpose of each sheep farm, and depends on age, weight and ability of the lamb to eat solid food⁴. According to the productive purpose, lambs can be weaned from 24 h postpartum until the age of their natural weaning. Dairy farms maintain ewes and lambs together for 24 to 48 h to allow lambs to suckling colostrum, and then make an abrupt weaning⁴. On some farms of sheep milk, lambs continue accessing their mother during short periods of time, allowing a restricted suckling. Commonly, sheep meat and wool farmers wean their lambs between 60 to 150 d of age, but most often before 120 d, moment in which the lamb already increased the intake of solid food, and after the lactation peak that occurs in the 3rd to 4rd wk postpartum. In this case, farmers separate ewes and lambs without needing artificial rearing, making easier handling, and reducing costs.

Stress response to artificial weaning

The abrupt and complete separation of the lambs before the natural weaning age is a stressful situation for ewes and lambs, which is caused by different stressors: 1) Emotional, generated by the end of the mother-lamb bond; 2) Changes in the physical and social environment, since at least one of the two is housed in a new environment, often with other animals with which they had no previous contact; 3) End of suckling, which implies the end of the neurophysiological changes induced by suckling and 4) Nutritional change, generated by the loss of milk and its complete replacement by other food^2,10,30. The response of the animal is the result of these stressors altogether, but the relative importance of each one has been poorly studied. After separation, ewes and lambs increase the frequency of behaviors related to searching the other. There is an increase in the frequency of vocalizations⁹ and at the same time standing and walking, as well as pacing (when animals walk again and again at a distance of 1 to 2 m parallel to the fence, modifying the direction of back and forth continuously), behavior that in lambs is exclusively associated with the loss of the mother³⁰. The increase in the number of vocalizations and pacing are behavioral changes more closely related to the stress response to weaning. Usually these changes occur quickly, reaching their maximum frequency in few hours, and lasting 3 to 4 d. The rapid end of these behaviors could be related to their lack of effectiveness, since they generate important costs without achieving positive responses^10,31. In addition, the increase breeding of the ewe and the lamb search- related behaviors, both reduce the feeding and resting time: the animals spend less time laying, grazing and ruminating after weaning^10,30,32. In recently weaned lambs fed on pastures or with dairy substitutes, some lambs redirect the suckling behavior trying to suck from other lambs³³.

The loss of the mother as a result of weaning is a main factor in the response of lamb’s stress. Damian et al³⁰ compared the stress response of lambs at weaning if they were reared artificially with sheep’s milk supplied in artificial teats or reared by their mothers. At weaning and when artificial rearing ended, only the lambs who lost their mother paced, and walked and vocalized more, decreasing the time grazing. This shows that these behaviors are mainly affected by the loss of the mother, and to a lesser extent by the loss of milk suckling and the change of feeding as a whole.

Weaning also produces acute physiological changes indicators of stress in ewes and lambs, as a rapid increase in the serum concentration of cortisol^34,35, which is one of the main endocrine indicators of the stress response in sheep^36,37. The increase in the secretion of cortisol is associated with modulation of the immune response of the animal³⁸, since in ruminants, it has been reported that artificial weaning impairs immune function^39,40,41. Moreover, the amount of antibodies synthesized after an antigenic challenge is lower in the lambs during the postweaning than at other times ⁴². After weaning, there is an increase in the number of leukocytes⁸, and a decrease in the concentration of total proteins and globulins of the ewe¹⁰. As weaning is a stressful management that affects the immune system, the animals may be more susceptible to diseases. For example, lambs recently weaned and experimentally infected with Haemonchus contortus and Trichostrongylus colubriformis had more eggs of these parasites, lower hematocrit, and a posterior lower production of antibodies against these parasites than unweaned controls⁴³. It has also been reported that weaning naturally increases the excretion of coccidia oocysts^8,9.

Weaning also affects negatively the growth of the lambs, and if they are not artificially reared, this effect may be even greater in lambs weaned before ending the development of the rumen^44,45. This delay in growth could also be explained as a consequence of the worst immune status and increased susceptibility to gastrointestinal parasites, as well as changes of behavioral indicators of stress^8,30,43. In synthesis, the behavioral changes and the physiological responses have negative consequences both at production and on welfare of animals, so it is important to develop alternatives to decrease them.

Factors affecting the response to separation of the ewe and her lamb

There are many factors that can influence the intensity of the response to the separation of the ewes and their lambs, as age, sex, genetics and feeding of the sheep during pregnancy. The excitement and the frequency of vocalizations are greater after weaning lambs at 2 than at 4 mo⁶. The same authors observed the same behavioral changes, and a lower growth rate of the lambs when they weaned them at 13 to 16 wk⁴⁶.

The effect of age at weaning on the growth of the lambs has been widely studied^44,45,47,48. In general, the rate of growth is more affected when weaning is performed earlier, which is probably due to a slower adaptation to solid food intake in younger lambs⁴⁹. In addition, mortality rates at 210 d were greater in lambs weaned at 45 d than at 60 and 75 d⁵⁰. These results indicate that at a younger age, when the ewe-lamb bond is stronger, and lambs have a greater social and nutritional dependence, the negative effects of weaning on the lambs’ welfare are greater.

It has also been determined that female lambs have stronger lamb- ewe bonds and greater responses to stressors than male lambs^51,52,53. In domestic sheep without limitations in the availability of food, abrupt weaning affected more the susceptibility to parasites and the growth rate of females than males^5,9. On the other hand, mountain sheep lambs (Bighorn) males weaned 2 to 4 wk before the estimated time of the natural weaning, showed slower growth until puberty than those that remained with their mothers, but females were not affected⁵⁴. This study was performed in natural conditions, where changes in the quality and quantity of available nutrients change throughout the year, having periods with strong feed limitations. This, together with the greater growth rate and energy demand of males, could explain the difference between male and female lambs. In general, although it has been reported that there are differences in susceptibility to parasites and the response of the immune system according to the gender of the offspring^55,56,57 , information about the factors that differentially affect males and females in response to artificial weaning is still insufficient. Lambs of different breeds have different growth rates, implying different degrees of advance in their natural weaning, and therefore the response to artificial weaning. Rhoenschaf lambs vocalized more at weaning than Merino lambs⁵⁸, which can be explained by the greater body development of this last⁵⁸. Similarly, F1 Texel by Corriedale lambs showed greater body weight and more rumination after weaning than pure Corriedale lambs, despite being both reared by Corriedale mothers^59,60.

The feeding level of the mother during pregnancy or after parturition can also affect the response of the lambs at weaning. Important feed restriction during pregnancy adversely affects the mother-lamb bond at lambing⁶¹ delays mother-lamb recognition⁶², and may alter the natural weaning process. Recently, it was observed that ewes maintained with food restriction before conception until the last third of gestation had lower body weight during pregnancy and produced less milk in the postpartum⁷(Freitas-de-Melo A, Ungerfeld R and Pérez-Clariget R, unpublished data). Lambs born from feed- restricted ewes grazed more before weaning, vocalized less and presented minor changes in the concentrations of albumin after weaning⁶³ (Freitas-de-Melo A, Ungerfeld R and Pérez-Clariget R, unpublished data). Probably the lambs of ewes that had better nutrition during pregnancy were more stressed because they had more losses at weaning, since in addition to the mother, they lost a greater quantity of milk in an age in which consumption is still important. Another no opposed explanation is that lambs born from undernourished ewes had advanced their natural weaning process, since they presented a greater frequency of grazing before weaning probably to compensate the access to less milk amounts.

Types of artificial weaning

In sheep the available published scientific information relating ewe -lamb bond before weaning and the stress response is scarce. There are commonly four types of artificial weaning: abrupt, progressive, in steps with restriction of the time accessing the mother, and in steps through a fenceline. The most commonly applied type is abrupt weaning, with a complete separation of the ewe and her lamb so there is no visual, auditory or olfactory contact after weaning¹⁰.

Progressive weaning is the gradual separation of the ewe and her lamb to increase the time of separation until the complete separation. In this type of weaning, vocalizations increase in the first periods of temporary separation, but animals habituate to the separations, and therefore changes are not so intensive after definitive separation⁸. However, progressive weaning has caused a greater sensitivity to the infestation of parasites before and after definitive weaning⁸. According to these authors, the lambs had greater sensitivity to parasite infestation (weaning was done at 3 mo), so according to them, at this age is preferable to abrupt weaning so the increase in the infestation of parasites is not so great⁸.

In weaning through fences animals can communicate, and thus visual, auditory and olfactory contact is maintained before the final separation⁶⁴. However, in this method lambs vocalized more the day of weaning, indicating greater stress than after abrupt weaning. Although females weaned from this method weighed more after weaning, they presented a smaller increase of the amount of coccidia that those weaned abruptly⁹, indicating that the immune response was adversely affected after the abrupt weaning.

There are some studies in two-steps weaning, in which during the first period the lambs are barred from suckling of the lamb covering the udder of the ewe, and in a second stage is the definitive separation. The lambs thus weaned responded with less agitation and vocalized less than abruptly weaned lambs⁶.

Management to reduce the stress response to weaning

In addition to different types of weaning, there are some practices that can be applied before or after weaning to reduce the response of ewes and lambs. Intravaginal devices used to synchronize estrus that release progesterone reduce the ewe response to weaning¹⁰. With these treatments ewes vocalize and pace less frequently. In addition, the treatment moderated the decrease of total proteins concentration, due to a minor reduction of the globulin concentration. The values of serum globulins after weaning in the untreated ewes decreased more than in ewes treated, reaching levels of hipoglobulinemia, which could indicate a state of immuno-deficiency. Therefore, this treatment can reduce susceptibility to diseases of ewes after weaning.

Although this treatment reduced the stress response to weaning, its application is not practical, as the treatment is prolonged and expensive. For this reason, it was recently investigated whether treatment with injectable progesterone administered only the day of weaning reduces the response of stress in sheep, which would generate practical alternatives. This treatment reduced markedly the frequency of pacing and walking the day of weaning, and a tendency to reduce the frequency of vocalizations compared with the control group⁶⁵.

Other management that reduce the stress response is to induce estrus in the ewes by hormonal treatments the day of weaning, at the same time that rams are introduced³⁵. This management reduced the increase of vocalization frequency and the cortisol concentration at weaning, and may be easily included in accelerated lambing systems aimed to obtain pregnant ewes during the early postpartum period.

It is also important to consider the management of animals after weaning. The post-weaning social enrichment improves the welfare of lambs⁶⁶. The stress response of the lambs diminished when lambs remained for 1 h per day in close contact with a human who handled them gently (caressed them and spoke to them) after weaning, or if stayed in contact with two adult ewes. In addition, the animals who received these treatments of social enrichment grew more during the fattening period. At the end of the fattening period, the lambs that were in contact with the human immediately after weaned were less reactive to human manipulation.

Similarly, weaned lambs that grazed together with adult ewes presented a higher bite rate, and ruminated and grazed more than single weaned lambs⁶⁷. These results indicate that the presence of adult animals at weaning mitigates the negative effects of separation from the mother, improving the efficiency of grazing. However, this, rather than as part of social enrichment, can be part of a strategy of social facilitation accelerating feeding learning by the lambs. It was also noted that the provision of a protein supplementation after weaning reduced parasite infestation in ewes⁵, improving the animals’ welfare.

Synthesis

In summary, artificial weaning is a stressful event for both the ewe and lamb, affecting their health the welfare, and the productive results. While this handling is necessary to optimize the productive results, the development and implementation of management systems that reduce stress, in addition to promoting animal welfare, could have an even more positive impact on health and productive aspects. However, the available knowledge on how to reduce the negative effects of weaning is still scarce, especially considering that many of them are applicable only in specific production systems. The great variability of breeds existing in sheep productive systems makes it necessary to develop a range of tools that can impact according to the different conditions, but allowing in synthesis, to respond to the current demands of society and increase the efficiency of the production systems.