Hider species

Sheep and goats typically isolate themselves from the flock to give birth, and after birth when the new-born kid or lamb has nursed it lies down and sleeps. Then the mother may leave to graze. However, a tendency for the kid but not the lamb to remain immobile until the mother returns is one of the few features that distinguish the behaviour of the two species (Hersher et al., Reference Hersher, Richmond, Moore and Rheingold1963). Goats, similar to cows, are regarded as ‘hider’ species while sheep are regarded as a ‘follower’ species (Lent, Reference Lent and Geist1974) though see Geist (Reference Geist1971) for work with mountain sheep. Indeed, Edwards and Broom (Reference Edwards and Broom1982) found evidence of this hider tendency in housed cows where calves tend to seek a resting place at the perimeter of the calving pen. This ‘hiding’ trait may have relevance for the development of the maternal filial bond especially in a fostering context. The development of the mother young relationship in hider species should be slower than in follower species, and one can expect the relationship between the lamb and its mother to develop quickly. As a consequence, attempts at fostering may be more difficult with sheep.

Here the focus will be on two aspects of the cow–calf relationship: first, the development of maternal responsiveness or the orientation of the cow to care for her young and second, the development of the maternal bond/relationship between the cow and calf, with the ability to recognise each other. To understand the distinction between the two processes some landmark studies concerning maternal filial relationships in other species will be reviewed.

Imprinting

Young precocial birds and mammals will shortly after birth respond to a wide variety of objects. The process which restricts the social preferences to a specific object has been extensively studied, especially in birds, and is generally referred to as ‘imprinting’ (Bateson, Reference Bateson1966, Reference Bateson2017; Sluckin, Reference Sluckin1972; Bolhuis, Reference Bolhuis1991). Attention was drawn to this by Lorenz (Reference Lorenz1935, Reference Lorenz1937) who characterised imprinting as a special form of learning, that took place during a ‘critical period’ early in life of the young, and when complete the preferences formed were ‘irreversible’. Later the term ‘sensitive period’ was used. Imprinting was measured by exposing young precocial birds (species where the young are relatively mature and mobile from birth or hatching) such as chicks or ducklings in the first few days of life to an inanimate object, such as a coloured ball, suspended in its individual rearing pen. Some hours or days later the chicks preferences for that object was measured usually in a simultaneous choice test, with the familiar ball and an unfamiliar object such as a ball of a different colour or an object of a different shape. The chicks chose the familiar. It was later found that the characteristics of the objects used were important, including its colour and movement. The length of exposure to the object, being allowed to follow the object and the role of sound were all extensively studied (for review see Bateson, Reference Bateson1966). While Lorenz (Reference Lorenz1935) maintained that the biological function of imprinting was to enable individuals to recognise members of their own species rather than particular individuals, Bateson (Reference Bateson1966) did point out that visual imprinting may also be concerned with parental recognition in addition to species recognition. Research on filial imprinting progressed in what was effectively a laboratory setting, in the absence of mother hen. This research produced insights into the behavioural and neural mechanisms underlying the imprinting process (McCabe, Reference McCabe2019).

Predispositions

It was found that young domestic chicks have an innate preference, or a developing predisposition, to approach a model of a stuffed junglefowl (simulating an adult member of its own species) rather than an inanimate objects in a simultaneous choice test (Johnson et al., Reference Johnson, Bolhuis and Horn1985; Bolhuis, Reference Bolhuis1991; Johnson and Bolhuis, Reference Johnson, Bolhuis and Andrew1991; McCabe, Reference McCabe2019). When given a choice between an intact junglefowl and a scrambling or degrading junglefowl there was no preference until the chicks had a version of the fowl that lacked a head. Then, they preferred the stuffed junglefowl. When given a choice between the stuffed jungle fowl, a stuffed Gadwall duck (a different species) or a stuffed Polecat (a potential predator) there was no preference, (Johnson and Horn, Reference Johnson and Horn1988). Thus, the configuration of features associated with the head or face region were more important than the details of the features themselves (Johnson and Bolhuis, Reference Johnson, Bolhuis and Andrew1991). The predisposition is not species or even class specific (Bolhuis, Reference Bolhuis1991). The concern was with the development of a predisposition and not with recognition of a parent. It was concluded that there are at least two perceptual mechanisms underlying the development of filial systems in chicks. A predisposition to respond to the general features of the imprinting object and another that recognises the object. The predisposition is independent of training or exposure to the object, and is completed before the birds were 52 h old (for reviews and discussion see Horn, Reference Horn1985; Hogan and Bolhuis, Reference Hogan, Bolhuis, Bolhuis and Verhulst2009; Hogan, Reference Hogan2017; McCabe, Reference McCabe2019). Of general interest is the finding that young when first born have an expectation of the world or an a priori knowledge, and are prepared to deal with what one might call ecologically appropriate stimuli. In relation to our species of interest, calves are prepared or predisposed to engage in teat seeking and other appropriate behaviours soon after birth to facilitate their survival (Broom and Fraser, Reference Broom and Fraser2015). Can these predispositions inhibit or facilitate behavioural change?

Predispositions and the reversibility of imprinting

Bolhuis and Trooster (Reference Bolhuis and Trooster1988) compared chicks that had been exposed at day one to either a stuffed jungle fowl or a rotating red box for two hours. They soon preferred the object to which they were exposed in a simultaneous choice test. On day 2 they were exposed to the alternative object for two hours. They were then given a preference test. Chicks initially exposed to the red box now preferred the jungle fowl and the chicks initially exposed to the jungle fowl still preferred the junglefowl. Thus, the earlier imprinting preference was reversible in the group exposed to the red box (what we may call the ecologically irrelevant stimuli). Johnson and Bolhuis (Reference Johnson, Bolhuis and Andrew1991) distinguished between general predisposition (colour or shape of object) and specific predisposition (clusters of stimuli). In the experiment of Bolhuis and Trooster (Reference Bolhuis and Trooster1988), these two mechanisms are engaged, leading to the prediction (Bolhuis, Reference Bolhuis1991) that imprinting should be reversible when two naturalistic stimuli are used, citing the evidence of Kent (Reference Kent1987a) with live hens. In this study chicks hatched by a live hen which remained with her for the first 3 d of life preferred the familiar hen to a novel hen in a simultaneous choice test after 30 min of separation from mother hen. When subsequently exposed to another live hen for 3 d and tested again they preferred the second hen. The chicks' preference was not very stable as only four hours separation from the familiar hen, at day three of age, was sufficient for them to lose their ability to discriminate between their own mother and an alien hen (Kent, Reference Kent1987a). Thus the chicks' relationship with their mother is more plastic than earlier laboratory studies might have envisaged. However, the reader will note that the language of the science has changed as we move from ‘imprinting’ to the study of ‘relationships’. It is interesting to note that the chicks' recognition of their mother hen was based on auditory cues (the hens' maternal cluck vocalisation) and not visual cues (Kent, Reference Kent1987a, Reference Kent1989, Reference Kent1993). To complicate matters further, the hens were unable to discriminate between their own brood of chicks and an alien brood of chicks of a similar colour when the chicks were 3 d old (Kent, Reference Kent1992a). Further, hens when broody, were aggressive and kept at a greater distance from other hens than in the non-broody state. This demonstrated that the socio-ecological context need to be considered when studying the development and maintenance of the maternal–filial relationship (Kent, Reference Kent1992b) in fowl, and the same is known to be true of other animals.

From imprinting to relationships and attachments

Hinde (Reference Hinde1982) pointed out that despite the many studies of ‘imprinting’, little was known about the chick's attachment to its natural mother, i.e. the ‘relationship’. While progress has been made since 1982 the above work gives an indication of the complexity of the developmental processes and also how the developmental processes are more flexible than previously believed. Insights regarding predispositions, and the effects of maternal separation, have relevance for the study of maternal–filial relationship in the cow.

Even in geese (Anser anser), the species which inspired early imprinting studies, there is a growing appreciation of plasticity in the developmental process. The finding in geese that broods were larger than can be produced from a single clutch and the evidence of ‘adoption’ or ‘gang broods’ (having more than one set of parents) or ‘creche’ broods (with a mixture of parents, non–breeding adults and subadults) show that the development of parent young relationship is more complex than previously believed, with the mechanisms remaining unexplained (Kalmbach, Reference Kalmbach2006).

Ecological aspects of recognition

The study of parent-young recognition in bank swallows (Riparia riparia), an altricial species (where the young are incapable of moving around on their own soon after hatching) that nest in large colonies in close proximity to each other is insightful. Cross fostering techniques found that the development of signature calls in the young from age 14 d was crucial in facilitating the parents ability to discriminate own from alien young. Before 14 d of age, alien young transferred into the nest were accepted by adult birds as if they were their own (Beecher, Reference Beecher and Aslin1981; Beecher et al., Reference Beecher, Beecher and Hahn1981a, Reference Beecher, Beecher and Lumpkins1981b). More recent work with jackdaws (Corvus monedula), also an altricial species, found that nestlings even at 20 and 28 d old were still equally likely to produce vocal and postural begging responses to parents and nonparental calls though there were some indication that older nestlings do discriminate while still in the nest (Zandberg, et al., Reference Zandberg, Jolles, Boogert and Thornton2014). Thus, earlier views that imprinting in birds was fixed to a short period early in life have been tempered by experimental and observational findings. Chicks fail to discriminate between mother and an alien hen after only four hours separation on day three post hatching, yet they are prepared to approach another maternal hen (Kent, Reference Kent1987a). There is evidence of adoption and gang brooding in geese (Kalmbach, Reference Kalmbach2006). While in jackdaws and bank swallows, though their ‘imprinting’ process occurs later in post hatch development, evidence suggests there is potential for considerable flexibility in the ‘imprinting’ process. The generality of this flexibility is of importance in the applied farm animal context.

The ‘sensitive period’

Bateson and Hinde (Reference Bateson, Hinde and Bornstein1987) made the general point that sensitivity to certain types of experience changes throughout life. The term ‘critical period’ (Lorenz, Reference Lorenz1937) in the imprinting context was defined as a phase of susceptibility preceded and followed by a lack of susceptibility. This view was replaced by the term ‘sensitive period’ implying a phase of greater susceptibility preceded and followed by lower sensitivity, with more gradual transitions (Bateson and Hinde, Reference Bateson, Hinde and Bornstein1987). They conclude that the processes that underlie the end of the sensitive period for filial imprinting are different from those responsible for its onset. In the case of filial imprinting, social isolation lengthens the sensitive period (Bateson and Hinde, Reference Bateson, Hinde and Bornstein1987). In birds that are hatched naked, such as jackdaws and bank swallows (see above) the onset is much later post hatch than in precocial birds such as ducklings or chicks. Age from embryonic development rather than chronological age (age from hatching) was found to be a more reliable indicator of sensitivity to an imprinting stimuli in Peking ducklings (Gottlieb, Reference Gottlieb1961). This distinction between developmental and chronological age was later utilised to explain the lower levels of behavioural interactions between a cow with twin calves and a cow with a single calf. A single calf has a longer gestational period than twin calves and thus twins are developmentally younger than singles at a given post-partum age (Roy, Reference Roy1980). Thus one could expect twin calves to be less active than a single in the days after birth, and they are less active (Price, et al., Reference Price, Martinez and Coe1985, Reference Price, Smith, Thos and Anderson1986), though such differences in behaviour need not necessarily indicate a difference in the maternal bond/relationship between the cow and her calf (Kent, Reference Kent1987b). It should be pointed out that ‘relationships’ have an elusive quality. We infer the existence of relationships using choice tests or carefully designed observational studies. Behavioural measures can indicate the existence of a relationship but measuring the ‘strength’ of a relationship is a very different matter.

Bateson developed a model referred to as the ‘competitive exclusion’ model to explain the ending of the sensitive period. It maintains that imprinting is a preemptive, self-terminating process that narrows the social preferences to those that are familiar and, therefore, tends to prevent fresh experience from further modifying those preferences (Bateson, Reference Bateson1979, Reference Bateson and Immelmann1981). Bateson and Hinde (Reference Bateson, Hinde and Bornstein1987) point out that the concept of a sensitive period does not necessarily imply that the behavioural patterns in question cannot be influenced later in life and they cite evidence where trauma and stress have renewed the plasticity of behaviour, even if under limited circumstances. This should be born in mind when considering the cows response to separation from or the death of her own calf. Stockmen and scientists will be aware of circumstances where the cow does not remain with her calf after birth and such events can unwittingly help our understanding of the developmental processes involved in maternal bond formation. Deprivation studies did yield insights into the processes that underlie the development of normal patterns of behaviour. Maternal deprivation of young monkeys resulted in long term behavioural problems (Harlow and Zimmermann, Reference Harlow and Zimmermann1959) showing the importance of post birth contact between mother and young.

Maternal responsiveness and lessons from maternal behaviour in rodents

Changes in behaviour before, during and after parturition were intensively studied in rodents (Rosenblatt and Siegel, Reference Rosenblatt, Siegel and Elwood1983; Rosenblatt, Reference Rosenblatt, Krasnegor and Bridges1990) and the findings on the development of maternal responsiveness have application in other species. Maternal responsiveness is the orientation by the parent to approach and interact with stimuli of relevance to a maternal relationship, such as the retrieval of nest building material and young pups not necessarily their own. Maternal responsiveness can develop in pregnant and indeed non pregnant females when exposed to pups in a process called ‘sensitisation’. The hormonal correlates of this behaviour have been studied (for review see Rosenblatt and Siegel, Reference Rosenblatt, Siegel, Gubernick and Klopfer1981, Reference Rosenblatt, Siegel and Elwood1983). In general, maternal responsiveness appears late in pregnancy, as in the example of sheep accepting lambs that were not her own before she had given birth (Hersher et al., Reference Hersher, Richmond, Moore and Rheingold1963; Poindron and Le Neindre, Reference Poindron, Le Neindre, Rosenblatt, Hinde, Beer and Bushnel1980; Poindron and Levy, Reference Poindron, Levy, Krasnegor and Bridges1990). Cervical stimulation at birth stimulated the onset of maternal behaviour in sheep (Keverne, Reference Keverne1988) and additional cervical stimulation about two hours after parturition facilitated the acceptance of alien lambs (Keverne et al., Reference Keverne, Levy, Poindron and Lindsay1983; Kevern and Kendrick, Reference Kevern, Kendrick, Krasnegor and Bridges1990). However, when rodent pups were removed from the dam at birth, maternal responsiveness to pups in terms of retrieving and nest building was extinguished by two and 4 d respectively. On the other hand, if the pups remained with the mother for some hours after birth then the mother maintained her responsiveness, even after 4 d of separation (for review see Rosenblatt and Siegel, Reference Rosenblatt, Siegel and Elwood1983). Thus, experience with the pups after birth, and not just the endocrinological state of the mother, is important for the development and maintenance of maternal responsiveness at a later date. The development of maternal responsiveness is a necessary condition for the development of a maternal relationship, even if the two processes should in some circumstances coincide. We can expect animals, both parent and young, to be predisposed towards certain stimuli that are ecologically appropriate. Stimuli features of the young (e.g. amniotic fluid on the calf at birth) will stimulate grooming by the cow and the cows body features will facilitate teat seeking in the calf (Broom and Fraser, Reference Broom and Fraser2015) and these are relevant to the development of the cow–calf relationship. However, being responsive and being predisposed are different.

The development of the maternal filial bond; the necessity of early mother–young contact

Attachment is a special affectionate relationship between two individuals that is specific in its focus and endures over time. The object of the attachment serves psychological functions which others cannot substitute (Hinde, and Stevenson-Hinde, Reference Hinde, Stevenson-Hinde, Bateson and Hinde1976; Gubernick, Reference Gubernick and Gubernick1981). The salient features of such attachments are (a) the formation of a special relationship, with (b) a specific individual (c) towards whom certain behaviours are directed rather than towards other individuals. While the bond is not any of the behaviours, it is inferred from the behaviour. Therefore, while the behaviour might change the attachment is more or less constant and enduring. The strength of a bond cannot be directly measured, though its existence can be inferred as described by Gubernick (Reference Gubernick and Gubernick1981), who defines maternal attachment as ‘the preferential responding between parents and offspring as defined by various operational criteria’. The operational criteria include the preference for one individual over another, seeking and maintaining proximity to that figure, a response to brief separation from the attachment figure, a response to extended periods of separation, a response to reunion with the presumed attachment figure and, finally, the use of the attachment figure as a secure base to explore the world.

Maternal attachments have been studied in sheep and goats and the sensory mechanisms involved in recognition were identified. Klopfer et al. (Reference Klopfer, Adams and Klopfer1964) compared goats that had their young removed at birth (an ‘immediate separation group’) to a second group who were permitted five minutes post-partum contact with one of its young (the ‘prior contact group’). The young were then returned after either one two or three hours of separation. The immediately separated group rejected the kids on their return after only one hours separation while in the five minutes of contact group the mother accepted her kids after three hours of separation. Thus early contact is essential for the development of maternal responsiveness – at birth and after separation. Maternal responsiveness is a prerequisite for the development of the maternal bond. Shortly after birth two processes are engaged; the development of maternal responsiveness and the development of the maternal bond. Earlier work maintained that even five to ten minutes contact after birth was found to be sufficient to establish a maternal bond in goats and sheep (Hersher et al., Reference Hersher, Richmond, Moore and Rheingold1963), and Klopfer et al. (Reference Klopfer, Adams and Klopfer1964) extended this to show that five minutes contact enabled goats to discriminate between their own and alien kids. Thus, the goats were both responsive and discriminating – a maternal filial bond had been formed. However in these studies (Hersher et al., Reference Hersher, Richmond, Moore and Rheingold1963; Klopfer et al., Reference Klopfer, Adams and Klopfer1964) simultaneous choice tests were not employed and the acceptance/rejection criterion used did run the risk of confounding effects of the brief post birth experience on the mother and the young, when responsiveness and bond formation were both developing at the same time.

Maternal filial attachment in goats was viewed as specific, rapidly formed and fairly stable. Later studies questioned this certainty. After two hours post-partum separation multiparous domestic goats displayed maternal caretaking of their kids in contrast to first time mother goats. Thus previous maternal experience increased the probability of maternal responsiveness after post-partum deprivation of maternal contact in the multiparous goats (Lickliter, Reference Lickliter1982). Further, in a detailed study, mother goats given five minutes post-partum contact with their own kid, followed by one hour of separation generally failed to discriminate between her own and an alien kid in a choice test. The alien kid was accepted if it did not have contact with its own mother and that demonstrates maternal ‘imprinting’ in goats takes longer than previously reported (Gubernick et al., Reference Gubernick, Jones and Klopfer1979). This also shows that the status of the alien kid (in terms of the kids relationship with its mother) is important. While the development of maternal bonds are more malleable than might be assumed the processes involved must take account of the state of both participants in the relationship. The kid or calf will itself develop with time and its previous experience is important in a fostering context. Relationships are interactive and each participant will respond to the others behaviour, which in turn is dependent on each other's previous experience.

The cow–calf relationship; towards fostering

Rearing calves with their dams in the dairy cow herd is a current issue and there are challenges that need to be addressed (Johnsen et al., Reference Johnsen, Zipp, Kalber, de Passille, Knierim, Barth and Mejdell2016). The behavioural mechanisms underlying the development of the cow–calf relationship is of concern here.

Attempts at fostering calves onto nurse cows have included methods such as introducing the calf to be fostered as soon as possible after the birth of the cow's own calf (Hudson, and Mullord, Reference Hudson and Mullord1977; Le Neindre et al., Reference Le Neindre, Pettit and Garel1978; Nicoll, Reference Nicoll1982). This is an attempt to avoid the differential responding by the cow towards her own calf and her rejection of alien calves. Smearing the calf to be fostered with amniotic fluids while introducing it to the nurse cow as soon as possible after birth (Hudson, Reference Hudson1977), or blindfolding the cow while smearing the calf with neatsfoot oil or amniotic fluids (Crowley and Darby, Reference Crowley and Darby1971; Kiley, Reference Kiley1976; Le Neindre and Garel, Reference Le Neindre and Garel1979) have been used in an attempt to manage the sensory mechanisms involved in recognition. Such techniques involved introducing the additional calf when the cow retained her own calf from birth. The cow will in these circumstances be able to discriminate her own from an alien calf.

These techniques focused on acting quickly before a specific bond was formed. The use of substances can reduce recognition cues. Odour transfer techniques involved the use of a cloth covering on the cows own calf shortly after birth and then 48–96 h later transferring it to an alien calf. Then the alien calf was substituted for the cows own calf. This method did facilitate fostering though such techniques require much skill and competent personnel (Dunn, et al., Reference Dunn, Price and Katz1987). The use of a hessian sack worn by the calf for 4 d and then transferred to an alien calf was assessed in a cross mothering context with beef calves between five and 16 d old (Herd, Reference Herd1988). This requires considerable amounts of effort on behalf of the assistant.

These fostering techniques reflect an awareness that the relationship between the cow and calf will have already formed. The competitive exclusion model which maintains that imprinting is a preemptive, self-terminating process and narrows the social preferences to those that are familiar, and prevents fresh experience from further modifying those social preferences (Bateson, Reference Bateson1979, Reference Bateson and Immelmann1981) applies here. The cow has already developed a relationship with her own calf and vice versa and the windows of the developmental train in Bateson's (Reference Bateson1979) model are closing.

In rodents, though an altricial species, the removal of pups for 4 d after some time with her pups resulted in the mother maintaining her responsiveness (Rosenblatt and Siegel, Reference Rosenblatt, Siegel and Elwood1983). In goats given five minutes post-partum contact with their own kid, and followed by one hour of separation resulted in the mother goat accepting her own and an alien kid after the one hour separation, provided that the alien kid did not have contact with its own mother (Gubernick et al., Reference Gubernick, Jones and Klopfer1979). This suggests that the so called ‘imprinting’ is more plastic than previously believed, because in these studies maternal responsiveness was maintained after the relatively brief separation. The period of separation resulted in the loss of recognition, as Kent (1987a) had found with chicks after 4 h of separation from mother hen.

Kent (Reference Kent1984) used a technique to enable cows to foster calves including her own at 4 d post-partum. Briefly and in general the dairy cow spent the first 24 h post-partum with her calf. The calf was then removed from the cow for three to 4 d whilst the cow was milked in the dairy herd. Then three to four calves were presented to the cow and her own calve could be among them. When this technique was followed, fostering was possible. While the sample size was small the results are best understood in the light of findings described above. The first 24 h cow–calf contact was important for the development and maintenance of maternal responsiveness in the cow after the three to 4 d of cow–calf separation. Maternal bond formation would have taken place during this 24 h of contact with the calf. After the separation the cow failed to discriminate between her own calf and an alien calf but she was still responsive to calves. Maternal responsiveness was maintained after the separation in the form of a preparedness to accept calves, including alien calves, of an appropriate developmental state.

Future directions

To understand the development of the cow–calf relationship it is wise to first explore the literature on maternal behaviour with other species. Considerable experimental and observational research has taken place over many years and with different species giving insights into the complex behavioural mechanisms that underlie maternal behaviour. These behavioural mechanisms have evolved over millennia and persist despite selective breeding and domestication. Ideas about sensitive periods did yield fruitful research programmes and the results of these studies should improving our understanding, and help prevent making conceptual errors when designing research programmes, in an applied animal behaviour context.

We have seen that animals are predisposed to approach ecologically appropriate stimuli such as facial-like features of the parent and post natal experience is necessary to shape the appropriate responses. Research work on the maternal behaviour of the cow could be described as sparse. This is in part due to the size of these animals that give birth once per year constraining what can be achieved in a research context with a limited number of animals. As seen above, experimental work with chicks did help overcome some economic constraints in testing hypotheses on maternal responsiveness and recognition after separation. Much work needs to be done with cows to first understand the behavioural mechanisms involved in the maternal behaviour and to understand behavioural needs of the cow and the calf and explore the development of fostering techniques that would improve the welfare of the cow and calf and indeed the welfare of those who work with and depend on these animals. For example, one would expect the cows responsiveness to calves would change at oestrus when the cows endocrinological profile also changes. Carefully designed non-invasive endocrinological work coupled with well-designed observational studies should yield fruitful insights. Such work should help improve the welfare of the cow and the calf.