Maternal deprivation and the development of stereotypic behaviour

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Abstract

Many farm, laboratory, zoo and companion animals experience some form of maternal deprivation. This is typically via separation from their mothers earlier than would happen in free-living populations, in some cases even while young are still dependent upon milk. Maternal deprivation may also occur in a qualitative way, via inadequate maternal care, perhaps caused by inexperience or by restrictive environments that limit maternal behaviours. In this paper we review evidence on the link between early separation from the mother and abnormal behaviour from a wide range of sources, including the early primate studies in this field, more recent examples from zoo and commercially reared animals, and human examples from studies of institutionalised children. We discuss factors that seem to influence the magnitude of later effects, such as developmental stage and age at separation, and whether separation is gradual (i.e. more similar to natural separation) or abrupt (as often the case in captivity). In these instances, however, maternal deprivation is just one aspect of a suite of changes that occur when infants are separated from their mothers. In the second part of the paper we therefore review the few cases where maternal loss per se has been investigated, and studies showing lasting affects of qualitative aspects of maternal care. We then look at the possible mechanisms underlying maternal deprivation-induced stereotypic behaviours including potential frustration of specific motivations, and lasting, more pervasive changes for instance in temperament or motor control. Finally, we discuss the practical and welfare implications of the effects of maternal deprivation, and suggest some topics for future research.

Introduction

Maternal deprivation is widespread among captive animals, particularly in the form of separation from the mother earlier than would happen naturally. All commercially reared animals are separated from their mothers/parents before the age at which they would naturally leave their natal territory or social group in free-living conditions. Some animals are even removed from their mothers while still dependent on milk, perhaps within hours of birth, and others are denied any parental contact at all. The point at which animals are separated from their mothers/parents in commercial systems is typically called ‘weaning’ and in this paper we use it in this way (although we acknowledge that the term actually refers to the biological process during which animals naturally stop suckling from their mother (see Martin, 1984)). Thus, we use the term ‘early weaning’ to refer to earlier than standard weaning practices in captive situations. In this paper, we review the impact of weaning and similar manipulations on abnormal behaviour.

Earlier than natural weaning from the mother is particularly evident in commercially reared animals, where fast reproductive turnover is important for profit. For example, dairy calves may be separated from their mothers at only a few hours old (e.g. EPA, 2004a), yet cattle do not naturally wean their calves until 9–11 months (Reinhardt and Reinhardt, 1981, Veissier et al., 1990, Reinhardt, 2002). Farmed piglets are separated at 2–6 weeks old, yet under (semi-)natural conditions they may suckle until 3–4 months old (Jensen, 1986, Jensen and Stangel, 1992, Stolba and Wood-Gush, 1989, Petersen, 1994). Farmed mink are separated from their mothers at around 7 weeks, despite still showing some suckling at this age and not dispersing for at least another month under free-living conditions (indeed young females may not leave their mother until 10 or 11 months old – see Jeppesen et al., 2000, European Commission Report, 2001). Furthermore, poultry eggs are sent to hatcheries for incubation (see EPA, 2004b), eliminating completely parental contact that would normally extend for 5–12 weeks (McBride et al. 1969, cited by Perré et al., 2002). Curtailed maternal care is also found in research, companion and zoo animals, although typically less early in development. Here, infants are usually removed once they have stopped suckling, even though their natural dispersal age would be much later. For example, laboratory mice are typically separated from their mothers at 21 days, yet free-living mice would not naturally disperse from their parental territory until approximately 35–42 days (see Latham and Mason, 2004). Similarly, elephant calves are separated from their mothers almost as soon as they are weaned off her milk (at roughly 3 years) (Clubb and Mason, 2002), yet young males would not naturally leave the mother and natal herd until 7–12 years later (Eisenberg et al., 1971, Douglas-Hamilton, 1972, Sukumar, 1989), and females would naturally remain with their mother and natal herd for life (Moss and Poole, 1983, Sukumar, 1989).

Captive animals may additionally experience maternal deprivation of a qualitative nature, e.g. via poor quality maternal care. Early separation from their own parents and/or subsequent housing in unnatural social groupings may mean that females are not properly exposed to young infants or the parental behaviour of more experienced females prior to the birth of their own offspring. In some species, such females may then be inexperienced with their own infants (e.g. chimpanzees, Goodall and Toms, 2003). Hand-reared animals similarly do not experience true maternal behaviours, despite the efforts of their human surrogate parents, and this may become apparent in their later behaviour (Kreger et al., 2004, Kreger et al., 2005). Furthermore, captive females may be incapable of exhibiting some or all maternal behaviours. This may be due to the physical restraints of their environment—for example stall-housed sows cannot perform the sniffing and nose-to-nose behaviours exhibited by sows in unrestrained conditions (see Harris and Gonyou, 1998). Mothers may also not appropriately display maternal behaviours if the excessive performance of other behaviours, such as stereotypic behaviours, occupies much of their active time (e.g. Sørensen and Randrup, 1986). Finally, social species which display allo-parental care may, in captivity, be exposed to fewer ‘aunts’ (allomothers) or other helpers than would occur in nature (e.g. elephants, reviewed Clubb and Mason, 2002).

Maternal deprivation is thus a common part of early experience for captive animals. Could it play a role in a common response to captive conditions: stereotypic behaviour? Stereotypic behaviour has been defined as ‘repetitive, invariant and apparently functionless behaviour’ (e.g. Ödberg, 1978, Mason, 1991b, Mason, 1991c). Behaviours traditionally categorised as stereotypic under this definition are widespread among captive animals: we have estimated (Mason and Latham, 2004) that such behaviours are performed by at least 85 million animals worldwide each year. However, one of us (GM) has suggested recently that this definition should be updated, placing more emphasis on biological causal factors, and less on aspects of phenotype that are poorly specified (e.g. ‘invariant’) or hard to measure (e.g. the presence or absence of proximate function). Mason (2006a) suggests instead that stereotypic behaviours are ‘repetitive behaviours induced by frustration, repeated attempts to cope and/or CNS dysfunction’. Behaviours whose biological causal factors are unknown should instead be defined as abnormal repetitive behaviours (ARBs). Updating the definition in this way reflects more accurately how most people use the term in practice, and reflects why such behaviours are worthwhile topics for study (Mason, 2006a). This updated definition also allows us to be less concerned with benign examples of rhythmic behaviour, such as a dog chasing a ball or a cat kneading a pillow; and instead to include repetitive behaviours known to stem from some environmental deficit causing frustration or CNS dysfunction, such as belly-nosing in piglets and allo- and teat-sucking in calves, which have not previously been called stereotypic behaviours because of their rather variable and transient nature.

To answer the question of whether maternal deprivation plays a role in the development of stereotypic behaviour, we first review scenarios where maternal separation is part of a suite of changes that are imposed on an infant, particularly looking at studies of primates in the 1960's, reports of institutionalised children, studies of captive-born versus wild-caught individuals, and hand-rearing studies. In the next section we discuss factors that can influence the magnitude of these effects. Then in the following section we try to isolate the role of maternal deprivation per se, by reviewing the few cases where maternal loss or qualitative aspects of maternal care have specifically been investigated. We subsequently look at some of the mechanisms by which such early experiences can cause or enhance stereotypic behaviour. Finally, in the discussion we review the practical and welfare implications of such findings, and suggest topics for future research.

Section snippets

Evidence from primate studies involving maternal deprivation

The first scientific accounts of the lasting effects of maternal deprivation in animals stemmed from the research of Harlow et al. several decades ago. Young primates naturally have a long period of dependency on their mothers, who have important roles beyond the mere provision of milk, e.g. transporting the infants, providing comfort. Thus it is perhaps unsurprising that being deprived of maternal care has major effects, including promoting stereotypic behaviour. Here, we summarise a recent

Factors affecting the magnitude of early deprivation effects

Although it is tempting to focus on maternal deprivation being the cause of resulting behavioural changes, the assumption being that the younger the infant the greater the impact of maternal loss is, effects may instead reflect age-specific effects of novelty, acute stress, etc. Thus, below we look at the factors that may influence these behavioural effects.

The role of maternal deprivation per se

Despite the vast array of literature about the effect of ‘maternal deprivation’, very few experiments have actually addressed the question of the effects of the loss of the mother per se. Perhaps the closest study to this is that of brooded and non-brooded domestic fowl (Gallus gallus domesticus) by Perré et al. (2002). Perré et al. reared half of the chicks in small groups with broody hens (not their mothers) until the hens became indifferent to the chicks, at approximately 8 weeks, and were

How early deprivation leads to stereotypic behaviour

Stereotypic behaviours generally appear in normal individuals housed in unnatural, restrictive environments that cause them to perform the same behaviour time and time again. The repeated behaviour may be one that the animal is motivated to perform or it may substitute for a highly motivated behaviour, and over time the behaviour may become performed out of habit (see Mason and Latham, 2004, Mason, 2006a). In some cases, however, restrictive, unnatural environments can lead to life-long changes

Discussion

Typical husbandry practices expose most captive animals to maternal deprivation, through earlier-than-natural separation from the mother and/or inadequate maternal care. There is plenty of evidence that maternal deprivation can cause stereotypic behaviour in captive animals and children in poorly run institutions. Thus, earlier-than-natural separation from the mother can cause the immediate emergence of stereotypic behaviours, including belly-nosing in piglets, and/or the emergence of

Conclusion

Almost all captive animals experience some level of maternal deprivation, from the extreme primate experiments of Harlow, through earlier than natural separation from the mother in many commercially reared animals, to qualitative differences in maternal care due to environmental restrictions or inexperience. Such poor or limited mothering can produce physiological and behavioural changes that are inappropriate and undesirable in captive animals, and which indicate poor welfare and abnormal

Acknowledgements

We would like to thank Robert and Joan Hinde for inspiring and informing GJM's early interest in social experience. We also thank Tina Widowski and colleagues for allowing us a preview of their manuscript; Knut Bøe for A. Olsson's thesis and Uta von Borstel for the translation; and Kathy Carlstead, David Shepherdson, Megan Jones and Neville Pillay for their personal inputs to the manuscript.

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