Anita. Behav., 1991, 41, 1015-1037

Stereotypies: a critical review

G E O R G I A J. M A S O N Sub-department of Animal Behaviour, University of Cambridge, Madingley, Cambridge CB3 8AA, U.K.

(Received 19 March 1990; initial acceptance l May 1990," final acceptance 27 October 1990; MS. number: 3551)

Abstract. Stereotypies are repetitive, invariant behaviour patterns with no obvious goal or function. They seem to be restricted to captive animals, mentally ill or handicapped humans, and subjects given stimulant drugs. In this respect they are abnormal, although possibly the product of normal behavioural processes. Stereotypies are often associated with past or present sub-optimal aspects of the environment, and have been used as a welfare indicator. It has been hypothesized that stereotypies have beneficial consequences which reinforce their performance, although other means, such as positive feedback, may equally explain their persistence. Empirical evidence links them with lowered awareness of external events, and reduced arousal and distress. However, as most of this evidence is correlational it remains uncertain that the stereotypies are themselves the cause of coping. Furthermore, they are heterogeneous in source of origin, proximate causation and physical characteristics, and they change over time in important respects, becom- ing more readily elicited by a wider range of circumstances. Therefore the properties of one stereotypy are not necessarily those of another.

A stereotypy is a behaviour pattern that is repeti- Examples include rocking movements and repeti- tive, invariant and has no obvious goal or function tive vocalizations in institutionalized humans (e.g. (e.g. Fox 1965; Hutt & Hutt 1970; Odberg 1978; Stone 1964; Berkson 1967), bar-chewing in stalled Wiepkema et al. 1983). A bout of recurring move- sows, Sus scrofa domestica (e.g. Wiepkema et al. ments may be remarkably sustained (e.g. Odberg 1983), head-swinging in zoo-housed bears and 1986), and the animal may appear to have difficulty elephants (Dittrich 1984), pacing in captive fennec in stopping (Feldman & Green 1967; Cronin et al. foxes, Vulpes zerda (Odberg 1984a), eye-rolling in 1984). Bouts of stereotypy are themselves repeated veal calves, Bos primogenius taurus (Fraser & (e.g. Stolba et al. 1983), and may be as predictable Broom 1990), and jumping in caged bank voles, in time and place of performance as they are in Clethrionomys glareolus (Fentress 1977; Odberg morphology (e.g. Hediger 1950; Berkson 1967; 1986). Meyer-Holzapfe11968; Hinde 1970, page 556). The In this review I address three questions. (1) Are organization of a stereotypy appears only partially stereotypies 'abnormal'? (2) Do stereotypies indi- dependent on external stimuli (e.g. Berkson 1967), cate a welfare problem? (3) Does performing a particularly when performed at high speeds (e.g. stereotypy reward the animal? I then consider the Fentress 1977). With time, a stereotypy may differences in how authors characterize stereo- become independent of the stimulus that originally typies, and the problems raised by treating the elicited its performance (e.g. Levy 1944; Hinde activities covered by the term as though all are 1970, pp. 556-557). equivalent. Stereotypies often develop in animals faced with insoluble problems (Stolba et al. 1983; Wiepkema 1983). They are not all induced by the environment, S T E R E O T Y P I E S AS A B N O R M A L however. Some result from brain damage or psychi- B E H A V I O U R atric conditions (reviewed by Robbins & Sahakian 1981; Ridley & Baker 1982), and others from drugs In this section, I discuss the two meanings of abnor- such as d-amphetamine (e.g. Robbins 1976). mality and the way the word is applied to stereo- Stereotypies are diverse in nature. Form and typy. I then describe the ways in which stereotypies timing depend on the species and the eliciting situ- resemble normal behaviour patterns, and the impli- ation, and may differ between individuals. Stereo- cations these have for hypotheses concerning the typies also differ in repetitiveness and inflexibility. biological significance of stereotypies.

0003-3472/91/061015 + 23 $03.00/0 9 1991 The Association for the Study of Animal Behaviour 1015 1016 Animal Behaviour, 41, 6

Stereotypy is often labelled an 'abnormal' behav- may be adaptive even when uncommon or unique. iour, with the meaning of 'abnormal' left unspeci- Furthermore, in some respects even the most fied (e.g. Odberg 1978, 1987a; Cronin et al. 1984, bizarre stereotypy resembles behaviour patterns 1985; Hughes & Duncan 1988). This is a source of seen in the normal, healthy, free-living animal confusion, since the word can be used in two dis- (Hinde 1962). Such similarities mean that although tinct ways. It can mean literally 'away from the stereotypies might be pathological, they cannot be norm', in the sense of being statistically rare or prejudged as such solely on the grounds of their different from a chosen population (e.g. Meyer- unusual appearance. Holzapfel 1968; McMahon & McMahon 1983, page 29; Houpt 1987; Fraser & Broom 1990). It can Stereotypies and Normal Behaviour also mean lacking in function (e.g. Fraser 1968; McMahon & McMahon 1983, page 37) or causing Stereotypies resemble normal behaviour pat- harm to the animal (e.g. Schmidt 1982; McMahon terns in three respects. First, to be invariant and & McMahon 1983, page 37), perhaps because it resistant to change, i.e. stereotyped, is not unique to is the product of underlying pathology (e.g. stereotypies. The same is true of, for example, McFarland 1981; McMahon & McMahon 1983, grooming, drinking and displays (Hinde 1970; page 39). A behaviour pattern may be abnormal in Fentress 1977; Dawkins 1986; Groothuis 1989a). one or both senses. The rigidity ofstereotypies may in part be explained Whether a stereotypy is abnormal in the first by the unvarying nature of those environmental sense depends on what is selected as 'normal'. For factors that would otherwise modulate and control example, stereotypies may be the norm for a captive the behaviour (Morris 1966; Ridley & Baker 1982). population. When Harlow & Suomi (1971) wrote of However, inflexibility in behaviour also results 'normal' stereotypy levels, they meant those of lab- from repetition. This has been observed in stereo- oratory monkeys that had been reared in a group typies (e.g. Meyer-Holzapfel 1968; Fentress 1976; rather than in isolation. However, the majority of Cronin et al. 1984), and in normal behaviour (e.g. authors (e.g. Fox 1968; Luescher & Hurnik 1987; Lashley 1921; Miller et al. 1960, pp. 81-93; Morris Fraser & Broom 1990) take as the norm the animal 1966; Stolba et al. 1983; Groothuis 1989a). The living free or in naturalistic conditions in captivity. process underlying the progressive decrease in In this case stereotypies are abnormal, in the con- variability is that extrinsic factors become less text and frequency of their performance (Broom important in the control of the behaviour pattern 1983), and often in the form of the movements and although an external stimulus may remain the involved. trigger, the pattern comes to be self-organizing Are stereotypies also abnormal in the second, (Fentress 1977; Carpenter 1984). With the involve- maladaptive sense? They have been described as ment of information-processing systems minimized, 'pathological' by, for example, Odberg (1984b), the animal is free to direct its attention elsewhere and are sometimes the expression of central (Lashley 1921; Fentress 1976) and the action pat- nervous system dysfunction (e.g. Ridley & Baker tern can be performed faster than would be possible 1982; Broom 1983). However, except in cases if guided by sensory feedback (Lashley 1917, 1951; involving stereotypic drug self-administration Miller et al. 1960; Fentress 1976; Carpenter 1984). (Ellinwood & Kilbey 1975), self-mutilation or Fixity of performance is therefore particularly evi- severe weight loss, it is not clear that stereotypies dent in a state of high arousal (Fentress 1976, 1977), are maladaptive in themselves. when selectivity of attention (Warburton 1987) and Some assume that if stereotypies are abnormal in speed of behavioural response (Dantzer 1986; the first sense, they must also be abnormal in the Warburton 1987) increase. second. The argument is that stereotypies cannot be A second feature that a stereotypy shares with the product of natural selection (they seem to be normal bebaviour is that, once developed, it may absent in the wild), nor of selective breeding for become independent of its original eliciting stimu- captivity (they are not unique to domesticated lus. It may then be displayed in a range of different species). Hence stereotypies cannot possibly be of situations (Hinde 1962, 1970, pp. 556-558; Odberg any benefit and, because they involve time and 1978, 1987a; Dantzer 1986). For example, a captive energy, can only represent a net cost to the animal. dingo, Canis dingo, would perform a stereotyped However, a learnt behaviour pattern, for example, head movement when pacing, with every change in Mason: Stereotypies reviewed 1017 direction. In time, this head-swing came to be not necessarily pathological, reason) they may shown whenever the animal made any turning- become inflexible, particularly in a highly aroused away movement (Fox 1971). With repetition, func- animal. Only if the costs of their performance tional behaviour, too, can show ease of elicitation demonstrably outweigh any benefits, or if they are (Hinde 1970, page 557; Dantzer 1986, 1989) and shown to result from a pathological condition, can autonomy from the original context (e.g. Baerends one say for sure that stereotypies are abnormal in 1975). For example, the display of the young black- the maladaptive sense. headed gull, Larus ridibundus, develops during agonistic encounters, but by adulthood it is no longer exclusively coupled with aggressive behav- S T E R E O T Y P I E S A N D P O O R iour, and is shown in a range of circumstances W E L F A R E (Groothuis 1989b). A third important, and apparently 'abnormal', Stereotypies have long been thought to indicate characteristic of stereotypy is that it has no obvious that an animal's environment is sub-optimal (e.g. goal, end-point or function. This need not, how- Hediger 1950; Broom 1983; Luescher & Hurnik ever, indicate that the behaviour is pathological, as 1987; Odberg 1987a), and that the animal is suffer- normal behaviour, too, can persist when appar- ing from a welfare problem (e.g. Broom 1983; ently devoid of functional consequences. Habits, Wiepkema 1983 reviewed by Odberg 1987a; Fraser for example, are actions that are relatively indepen- & Broom 1990), such as stress (e.g. Vestergaard dent of the current value of their original goal 1981; Anonymous 1989). (Dickinson 1985). Foraging behaviour (Duncan & This view is based on several features of stereo- Hughes 1972; Wood-Gush et al. 1983; Anderson & typies: the contexts in which they develop; the Chamove 1984) and operant responses (Neuringer behaviour patterns from which they arise; the 1969; Singh 1970; Duncan & Hughes 1972; factors that influence their development and Markowitz 1982) may be performed even when subsequent performance; and the fact that some food is supplied freely, and behaviour used in stereotypies involve self-damage. This evidence is avoiding aversive stimuli will persist even when outlined below. punishment stops (Hinde 1962; Solomon 1967). One suggested explanation is that the behaviour The Contexts of Stereotypy Development pattern is reinforcing in its own right (e.g. Wood-Gush 1963; Hinde & Steel 1972; Roper Stereotypies are often physically and temporally 1976; reviewed by Hughes & Duncan 1988). linked to sub-optimal features of the environment. Alternatively, the apparently inconsequential Specifically, they develop in the following types of behaviour may result in benefits that have not been situation (types that are not mutually exclusive; identified, perhaps because they are evident only fear may involve frustration if the animal cannot over a longer timescale (this tends to be assumed for escape, and so on). play and sleep, for example; see reviews by Martin & Caro 1985 and McFartand 1989). Frustration Situations in which an animal is motivated to Conclusion perform a behaviour pattern but is unable to do so, If one takes the free-living healthy animal as the are frustrating (Hinde 1970, page 414; Duncan & norm, then stereotypies are in one sense abnormal: Wood-Gush 1972). They tend to result in displace- they seem restricted to captive or psychologically ment or redirected activities (see McFarland 1985, impaired individuals. However, one cannot infer page 384, for an account of displacement activities), from this that stereotypies are necessarily function- or, if the problem is repeated or chronic, stereo- less or pathological, particularly as even the typies (Duncan & Wood-Gush 1972; Broom 1983; strangest of stereotypies may result from perfectly Wiepkema 1983, 1987; Salzen 1990). Frustration is normal phenomena. Specific behaviour patterns aversive (Duncan & Wood-Gush 1974; Dawkins are often elicited by situations of stress, conflict, 1990). frustration and the imminent arrival of food, and if Examples include the stereotypic pacing devel- these are repeated (for whatever mysterious, but oped by laying hens, Gallus gallus domesticus, with 1018 Animal Behaviour, 41, 6 no access to a suitable nest-site (Duncan 1970; Meyer-Holzapfel 1968; Dantzer 1986; Dellmeier Wood-Gush 1972), and in association with intense 1989); or because it involves the lack of several food frustration (Duncan & Wood-Gush 1972). specific factors (e.g. Keiper 1969), and hence the Stereotypy can sometimes be reduced by providing frustration of several motivations. Stereotypies the appropriate extrinsic factors (e.g. Meyer- that are more evident in barren than complex Holzapfel 1968; Stevenson 1983; Appleby & environments have been observed in a number of Lawrence 1987), or artificial substitutes to which species (e.g. Levy 1944; Berkson 1967; Norgaard- the behaviour can be redirected (e.g. Schmidt Nielsen 1984; Odberg 1987b; Bryant et al. 1989), 1982). and rocking stereotypies are more common in blind than sighted mentally handicapped humans (Berkson & Davenport 1962, cited in Hinde 1970, Unavoidable stress or fear page 557). The closer the confinement, the greater Examples of stereotypies associated with stress- the stereotypy developed by sows, for example ful or arousing situations include the leg-swinging (Vestergaard 1981; Broom & Potter 1984), rhesus of children doing abstract homework (Soussignan macaques, Macacca mulatta (Draper & Bernstein & Koch 1985); the stereotypic vomiting and sway- 1963) and bank voles (Odberg 1987b). If an animal ing of a female sloth bear, Melursus ursinus, in the is isolation-reared in an impoverished environment presence of an aggressive male (Meyer-Holzapfel (e.g. Berkson 1967), the stereotypies it develops 1968); and the stereotypies such as body-rocking resemble those of a range of clinical conditions, shown by the mentally handicapped when dis- including autism, schizophrenia, mental retar- tressed (e.g. Stone 1964). The location ofstereotypy dation and organic brain damage (e.g. Stone 1964; performance may sometimes reflect the stressful Berkson 1967; reviewed by Robbins & Sahakian nature of the causal factors: deprivation-reared 1981). Such stereotypies are very persistent, and monkeys retreat to the same part of the cage to may indicate the initial challenge to have been so perform stereotypies as they do to sleep, or to hide severe that the effects on the central nervous system (Berkson 1967). That a tranquillizer will inhibit the are long-lasting, perhaps irreversible (Ridley & development of stereotypic pacing in the hen has Baker 1982). been suggested as indicating the role of fear (Duncan & Wood-Gush 1974). However, the agent Behaviour Patterns from which Stereotypies used, reserpine, is a major, or anti-psychotic, tran- Develop quillizer, and as such has many effects besides fear reduction (e.g. Rech & Moore 197t). Interpretation Stereotypies develop from a range of behaviour of these results is therefore problematic. Interest- patterns. The nature of its source behaviour pattern ingly, Munkvad & Randrup (1966) found major is often evident in the physical appearance of a tranquillizers to block amphetamine-induced stereotypy. These source behaviour patterns may stereotypies, but minor tranquillizers (sedative, themselves suggest that what causes the stereotypy anxiolytic agents) to have no effect. is to the detriment of an animal's welfare. For example, they include displacement activities, adjunctive behaviour (i.e. the behaviour displayed Restraint and lack of stimulation by an intermittently reinforced animal whenever Stereotypies have been associated with barren the probability of reinforcement is low; Falk 1971), and restrictive conditions by, for example, Levy and intention, vacuum and redirected movements (1944), Hediger (1955), Morris (1964), Meyer- (e.g. Levy 1944; Rushen 1984, 1985; Odberg Holzapfel (1968) and Hinde (1970). This type of 1987a), behaviour that is classically associated with environment is thought to be sub-optimal (e.g. frustration, thwarting, or a conflict of motivations Stolba et al. 1983; Wood-Gush et al. 1983), perhaps (see e.g. McFarland 1985). The stereotypies of because there is a need for sensory stimulation per some captive animals develop from what appear to se (e.g. Petrie 1986, cited in Dellmeier 1989); be intention movements of escape (Hinde 1962; because arousal needs to be kept within optimal Meyer-Holzapfel 1968; Duncan & Wood-Gush limits (Ewbank 1973; Hennessy & Levine 1979; 1972; Odberg 1986). Pacing may also arise from reviewed by Inglis 1983 and Toates 1983); because thwarted intention movements of approach to con- locomotor movement is constrained (Levy 1944; specifics (Meyer-Holzapfel 1968; Odberg 1978) or Mason: Stereotypies reviewed 1019 prey species (Stevenson 1983). 'Yawning' and frequency on exposure to a novel object or loud head-shaking stereotypies in hens develop from dis- noise, or disturbance by a human (e.g. Berkson et placement activities shown in conflict situations al. 1963; Meyer-Holzapfel 1968; Fentress 1976; (Norgaard-Nielsen 1984), or alerting activities Hughes 1980; Kiley-Worthington 1983). If the performed in the presence of disturbing stimuli stimulus is very intense the stereotypy may be inter- (Hughes 1983). Stevenson (1983) explained the rupted, the animal performing instead an appropri- form of some stereotypies, such as pacing in a circle ate orientation or flight response. However, the or figure-of-eight, as arising from two conflicting stereotypy may be performed at a greater intensity motivations, the animal alternately approaching, when resumed (Fentress 1977). then retreating. Factors that slow, reduce or eliminate stereotypy are those that, in contrast, give the animal the Factors Affecting Stereotypy Development opportunity to perform other behaviour patterns (e.g. Berkson 1967; Keiper 1970) or that decrease Stereotypies elicited by one aspect of the environ- arousal (Berkson 1967). For example, bank voles ment may have their development enhanced by perform less stereotypy if moved from a small cage another. Potentiating factors involve, in general, to a bigger and more enriched enclosure (Odberg frustration, stress, or lack of control. For example, 1987b). The stereotypies of isolation-reared stereotypy is greater in single-housed than in chimpanzees decrease with arousal-reducing drugs group-housed sheep, Ov& aries, and is increased by (Fitz-Gerald 1964, cited in Berkson 1967), and in a a restriction in dietary intake (Marsden & Wood- novel environment stereotypy performance falls as Gush 1986). Isolation-rearing (Sahakian et al. the animal habituates (Berkson & Mason 1964). 1975; Jones et al. 1988), uncontrollable footshock (MacLennan & Maier 1983), food deprivation Stereotypies and Self-damage (reported MacLennan & Maier 1983) and repeated Examples of stereotypies involving self-damage restraint-stress (Cabib et al. 1984) can potentiate include self-biting (Berkson 1968; Broom 1983) and the stereotypy-inducing effects of psychomotor eye-poking by autistics (reported Ridley & Baker stimulant drugs. Heightened susceptibility to stress 1982). Stereotyped weaving and stall-walking by may predispose an individual to stereotypy; reac- horses can cause weight loss and painful back con- tive, sensitive horses, Equus caballus, are more ditions (Fraser 1980; Fraser & Broom 1990). Wind- prone to the development of stereotypy than sucking and crib-biting also reduce the condition of 'phlegmatic' breeds (although a major confounding stabled horses (Fraser 1980; Kiley-Worthington factor here is that the former are often stabled 1983); wind-sucking can lead to gastro-intestinal more intensively; Kiley-Worthington 1983), and catarrh, colic and reduced food intake (Dodman et stress levels may be behind the great individual al. 1987; Houpt 1987; Fraser & Broom 1990), and differences in human response to amphetamine crib-biting to tooth-wear (Broom 1983; Dodman et (MacLennan & Maier 1983). al. 1987; Houpt 1987) and the ingestion of splinters (Dellmeier 1989). Repeated contact of the body Factors Affecting Stereotypy Performance with cage walls or bars during stereotypy may cause Factors other than the original causal sl imuli can sores (Morris 1964; Meyer-Holzapfel 1968; Odberg trigger, prolong or increase the rate of re ~etition of 1986), or impact injury (Fraser & Broom 1990). an established stereotypy. Again, these eliciting or The detrimental effects ofstereotypy are not exclus- enhancing events are often stressful or frustrating ively physical: the stereotypies of autistic children (e.g. Fox 1984). For example caged mink, Mustela may prevent learning and social interaction vison, perform their stereotypies when paired and (Lovaas et al. 1971). wanting to flee (de Jonge & Carlstead 1987). Stress can reinstate the symptoms of amphetamine- Conclusion intoxication in abstinent humans (reported Overall, stereotypies are often seen in environ- MacLennan & Maier 1983). In the laboratory- ments that seem sub-optimal (though this must be housed chimpanzee, Pan troglodytes, stereotypy is demonstrated independently of the presence of potentiated by hunger (Berkson & Mason 1964) stereotypy, to avoid circularity). They are physi- and low levels of stimulation (Berkson 1967). In a cally or temporally associated with lack of stimu- range of species, stereotypies increase in rate and lation, or events such as acute stressors or the 1020 Animal Behaviour, 41, 6

expected arrival of food. All these environments Once developed, stereotypies are remarkably may involve chronic conflict and frustration persistent, and this could indicate that performance (Odberg 1978, 1987b) and hence stress (e.g. Falk has some reinforcing value (e.g. Duncan & Wood- 1971; Duncan & Wood-Gush 1974; Brett & Levine Gush 1972; Odberg 1987a). Stereotypies can 1979), particularly if uncontrollable or unpredict- remain unextinguished over long periods of time, able (e.g. Weiss 1971; Reynolds 1978; Dantzer et al. e.g. blind, retarded children may spend their days 1983; Herbert 1987). Other stereotypies are rela- engaged in the same stereotypies at 15 as at the age tively independent of the current environment, but of 2 (Stone 1964). Stereotypy levels may even reflect a past challenge severe enough to have increase in performance over time, as they do, for traumatic effects on the central nervous system. example, in repeatedly tethered sows (e.g. Wood- Thus the acquisition of stereotypies indicates an Gush et al. 1983) and tong-term inmates of mental environment that is probably inadequate, and as institutions (Berkson 1967). Stereotypies that such, presumably aversive. Does current perform- animals appear to have copied from others, for ance therefore also indicate current suffering? It is example, the spot-pecking of pigeons, Columba certainly possible (e.g. Fraser 1990), but not all livia, placed adjacent to birds already showing this agree (e.g. Dantzer 1986, 1989). Without knowing stereotypy, can persist even when the original what the consequences of performance are, for 'tutors' are absent (Palya & Zacny 1980). Some example, one cannot infer that this is necessarily the stereotypies persist despite an energy cost. Stereo- case. typic sows, for example, use more energy than non- stereotypic animals (Cronin et al. 1986a). Also S T E R E O T Y P Y AS A R E I N F O R C E R consistent with reinforcement (see the argument of Warden et al. 1935, cited by Dawkins 1990) is the It has been argued that performing a stereotypy difficulty of deterring an animal from performing a rewards or reinforces the animal (e.g. Fox 1965, stereotypy. For example, aversive conditioning will 1971). This is despite the behaviour's lack of appar- not cure horses of pawing (Fraser & Broom 1990). ent goal or function. The idea has arisen for two Some horses continue to wind-suck even if they reasons. First, features of stereotypies suggest have to work against a strap fitted around the reinforcement. Second, empirical evidence associ- throat, and may give themselves pressure sores ates stereotypy with states that the animal might in the process (Fraser & Broom 1990). The many find rewarding. The evidence for the reinforcing cases of individuals persisting in stereotypy even nature of stereotypy, the hypothesized reinforcers when the behaviour results in self-damage have for stereotypy and the evidence supporting some of prompted suggestions that stereotypy is a 'need' these hypotheses, are discussed in the following (Odberg 1986). Similarly, adjunctive polydipsia sections. Adjunctive behaviour is included in this (excessive drinking) is difficult to discourage with discussion because it gives rise to some stereotypies punishment, even more so than deprivation- (e.g. Rushen 1984). I conclude by discussing the induced drinking (Falk 1971). Stereotypies may be implications of a reinforcing stereotypy for the so persistent that rewarding alternative behaviour long-term benefit of the animal. patterns has little effect. For example, rats, Rattus norvegicus, on a schedule of random reward and Evidence for Reinforcement punishment develop a jumping movement that That stereotypies develop over a period of time persists even when the regimen is changed so that (e.g. Meyer-Holzapfel 1968; Palya & Zacny 1980; the problem is soluble (Feldman & Green 1967; Cronin & Wiepkema 1984), rather than being Liberson 1967). Unfortunately, persistence may be immediate responses to the eliciting situation, has explained by means other than reinforcement. been taken by some (Blackshaw & McVeigh 1984; A number of other processes could give rise to Cronin et al. 1986a) as indicating that they are persistent behaviour. For example, a behaviour learnt, reinforced, behaviour patterns. For similar pattern may be maintained by the constant pres- developmental reasons adjunctive behaviour has ence of releasing stimuli, combined with a lack of also been suggested as a learnt response (Roper behavioural competition from other motivational 1980; Rushen 1984). However, sensitization, or systems (Hediger 1950; Morris 1964). The persist- some other progressive change in the central ence of some environment-induced stereotypies has nervous system, is an alternative explanation. been further explained in terms of positive feedback Mason: Stereotypies reviewed 1021 from appetitive behaviour patterns upon the motiv- removing the animal from the eliciting situation ational bases for their own performance (Dantzer (Odberg 1989). For example, stereotypy has been 1986; Hughes & Duncan 1988). These patterns, suggested as relieving anxiety (Fox 1965). such as biting movements in intensively housed The hypothesized means of effecting coping fall pigs, therefore persist as long as the extrinsic factors into three main types, discussed in this section. necessary for consummation, food, for example, Some of the hypotheses have empirical support. I remain absent. Whatever the original reasons for survey this in the following section. repeating a behaviour pattern, repetition itself can Implicit in the first type of hypothesis is that the strengthen performance, by sensitizing the neuronal original, source behaviour pattern is reinforcing, pathways involved (as discussed above; Dantzer and so is repeated by the animal. The stereotyped 1986, 1989). This decreases the ability to shift nature of the resulting behaviour is no more than a behavioural programmes (Dantzer 1989): the ani- by-product of this repetition. Among hypotheses of mal becomes locked into a repeated sequence of this type are that the performance per se is import- movements. Raised arousal is a fourth possible ant: the behaviour is suggested to be reinforcing in cause of persistence (see Fentress 1976). Finally, an its own right, perhaps by providing an outlet for a explanation for the persistent stereotypies induced specific behavioural 'need'. Wiepkema (1985), for by stimulant drugs is that they are by-products of example, suggested that oral behaviour directed at drug-induced neurological 'over-activation' (Lyon the bars of a cage can substitute for normal, & Robbins 1975; Robbins 1982). Reinforcement consummatory activity (although whether it is an need not always be invoked to account for the adequate substitute is open to question). In persistent nature of stereotypies, and therefore thwarted hens, the pacing that develops next to the persistence alone is not sufficient evidence that the cage door, apparently from attempts to escape, will behaviour is reinforced. persist even after the door is opened. It has been More convincing evidence for the reinforcement suggested that the stereotypy might be an adequate of stereotypies is that animals sometimes appear to substitute for real escape (Duncan & Wood-Gush work in order to allow performance. For example a 1972), although of course the persistence may be mental patient whose stereotypy involved swinging explained in other ways (as previously discussed). a certain toy constructed a replacement one when Alternatively, it may be that the consequences of this was removed (Berkson 1964). A dominant ani- the behaviour are important. For example, stereo- mal may chase a subordinate away from the spot typic tongue-playing in calves might stimulate the favoured for pacing in order to perform this stereo- production of saliva, or increase feelings of satiety typy itself (Odberg 1984a), or push another out of (Wiepkema et al. 1987); bill-shaking in chicks might its way in order to complete a stereotypic move- have a role in preparing the animal for another ment (Horsmann 1986). Similarly, on an intermit- activity (Forrester 1980); and some stereotypies of tent feeding regime, animals will work for the autistics may be a means of non-verbal communi- chance to perform adjunctive behaviour such as cation (Garrigues et al. 1982). The exteroceptive or polydipsia or aggression (Falk 1971). proprioceptive sensory input generated might be an Overall, it would seem that some forms of stereo- important, more general, consequence of perform- typy could be reinforced in some way, and that ance (Hinde 1962; reviewed by Berkson 1967; others develop and persist in a way that is at least Stolba et al. 1983; Wood-Gush et al. 1983). This consistent with reinforcement. Other mechanisms could come from rubbing against solid objects, as may well be involved, however. well as from the movement itself. Some stereo- typies, such as pacing next to parallel bars, may provide a stimulating flicker of light and shadow Consequences of Stereotypy (Fox 1971; Lovaas et al. 1971), and some rocking Several hypotheses have been advanced to stereotypies have been suggested as masturbatory explain the possible reinforcing nature of stereo- (Potter 1927, cited in Berkson 1967). Sensory input typy. They all propose, explicitly or implicitly, that may be rewarding in a dull, unstimulating environ- the reward value of stereotypy is that it is a coping ment (e.g. Hinde 1970, page 557; Bareham 1972; response, i.e. that it in some way keeps the animal Broom 1983, 1987). within optimal physiological or psychological Behaviour can be used to inhibit as well as to limits (Fraser & Broom 1990), without actually facilitate central nervous system activity (Forrester 1022 Animal Behaviour, 41, 6

1980). Stereotypy shown i_n an unpredictable, endorphin-release that occurs in times of stress or uncontrollable or otherwise arousing environment conflict (Cronin et al. 1986a; Broom t987). Such might be a means of reducing arousal (e.g. Hines explanations, however, fall down in cases where 1942, cited in Hinde 1970, page 558; Odberg 1978; the animal spontaneously changes the form of its Dantzer & Morm6de 1981; Cronin et al. 1986a). stereotypy. Stereotypy may lower responsiveness to external stimuli (e.g. Odberg 197.8; Broom 1987) or pain Evidence (de Lissavoy 1963), and focus attention away from the source of conflict (e.g. Kiley-Worthington In this section I review the circumstantial and 1977; Wiepkema 1982a, 1987). It might do this by empirical evidence for the hypotheses outlined activating sensory channels so that the processing above. I tackle first the specific hypotheses that of input from other sources is interfered with (e.g. stereotypy increases sensory input and arousal, Hutt et al. 1964; Lovaas et al. 1971; Rushen 1984; rewarding the animal; that it decreases arousal, Dantzer 1986). Thus the sensory input from stereo- perhaps by lowering responsiveness to external typy might, paradoxically, be rewarding in both stimuli; and that it results in a release of endogen- under- and over-stimulating environments (Stolba ous opioids. I then discuss the evidence for the gen- et al. 1983). Alternatively, endogenous opioids eral hypothesis that stereotypy is, by whatever might be involved in a stereotypy-mediated reduc- means, a coping response. I attempt to resolve the tion of responsiveness and arousal (e.g. Cronin apparent contradictions within the data, and dis- et al. 1986b; Broom 1987; Dodman et al. 1987; cuss the difficulties in interpreting results that Kennes et al. 1988). suggest that stereotypy is of no consequence at all. The second type of hypothesis considers the pre- Evidence that stereotypy has beneficial conse- dictable, repetitive nature of the behaviour to be quences is largely correlational. The studies either reinforcing. Some have linked stereotypies with the exploit natural variation within (or sometimes calming effects of being rhythmically rocked, between) populations, or focus on the changes cradled or groomed (Fox 1984, page 184), and the within individuals that accompany the develop- sleep-inducing effects of rhythmic audio-visual ment or performance of a stereotypy. Not all the stimulation and limb movement (Stone 1964). hypotheses have empirical support, however. Rhythmical stereotypies have been suggested as The use of stereotypy to increase sensory input, mimicking passive intra-uterine movements (Levy for example, is a hypothesis unsupported by data. 1944), a mother's heartbeats (Fitz-Herbert 1950, Although a plausible idea, given the performance cited in Berkson 1967), or the movements of of stereotypy in barren environments and the suckling (Freud 1905, cited in Thelen 1979). Stereo- descriptions of, for example, the 'self-stimulation' typy's repetitiveness and rigidity have been hypoth- behaviour ofautistics (Lovaas et al. 1971), it has yet esized to increase the average predictability of an to be shown that, with stereotypy, there is an otherwise unpredictable environment (Forrester increase in arousal dependent on sensory input. 1980; Broom 1981, page 99, 1983). The predictable Furthermore, the circumstances of the perform- outcome of repeating the movement may mean that ance of stereotypy may simply indicate that it the behaviour is no longer associated with emotion occurs when there is no over-riding tendency to do (Wiepkema 1987), a state that, in the contexts anything else (e.g. Hinde 1970). associated with stereotypy, the animal might find However, some evidence supports the idea that rewarding. stereotypy lowers arousal. For example, the stereo- In the third type of hypothesis, finally, the rein- typies of autistics are accompanied by increased forcer is not a genuine consequence of the behav- heart-rate variability, a response associated with iour but a coincidental event, superstitiously REM sleep and other states of low stimulus input associated with it by the animal. For example, (Hutt & Hutt 1978). Leg-swinging is associated the animal might repeat a pattern of behaviour with reduced heart rate in normal children superstitiously associated with the arrival of food (Soussignan & Koch 1985), and brain waves typical (Hinde 1962), the low arousal that might follow of drowsiness accompany the stereotypies of blind, moving to the 'sleeping area' of the cage (Berkson retarded children (Stone 1964). That the signifi- 1967), the performance of functional behaviour cance of a stereotypy may lie in its very persistence such as defaecation (Cronin et al. 1984), or the is suggested by this last study, which showed only Mason: Stereotypies reviewed 1023 protracted or intense bouts to be accompanied by signs of lowered arousal may be independent and the slowed brain waves. A relationship with de- simply coincidental. For example, stereotypies and arousal has also been found for some adjunctive or opioid-mediated analgesia both occur in the post- displacement activities (Marler & Ellen 1951, cited feeding period in sows, but there is no evidence that in Odberg 1989; Barnett 1955, cited in Fox 1965; the reduced sensitivity is caused by the behaviour Delius I967). Lowered arousal may stem from (Rushen et al. 1990). Similarly, where a stereotypy lowered responsiveness to external stimuli. is linked with decreased attention to external The association between stereotypies and factors, the former need not cause the latter: stereo- lowered responsiveness to the environment has typies and reduced attention may arise indepen- been made by, for example, Odberg (1978), Cronin dently from exposure to an environment that the et al. (1984) and Dantzer (1986). Lovaas et al. animal learns is unlikely to provide it with stimu- (1971) found that autistic children trained to lation (Wood-Gush et ah 1983); from high arousal approach a dispenser for a food reward at the (Fentress 1976; Warburton 1987); or from a strong sound of a tone, showed much longer response but frustrated motivation, the animal being un- latencies if engaged in stereotypy. Nodding in interested in anything save food, for example horses is associated with what appears to be a 'light (Wiepkema 1982b) and performing, in its frus- somnolent state' (Fraser & Broom 1990), and tration, repetitive adjunctive behaviour. An Stevenson (1983) describes the 'trance-like' state of alternative interpretation of the correlational data an alarmed and pacing animal as making the is that stereotypy is dependent on the processes behaviour almost impossible to interrupt. Simi- involved in coping. larly, the rocking stereotypies of institutionalized Thus it is important to distinguish between the humans are accompanied by a lowered awareness consequences of the stereotypy itself, and those of of external stimuli (Stone 1964; Berkson 1967), and the processes underlying it: a stereotypy could be a may even culminate in a coma-like condition symptom rather than a cause (e.g. Broom 1983). (Stone 1964). Low responsiveness may be evident For example, restriction of attention could be the even when the subject is not currently engaged in cause of stereotypies (Fentress 1976; see also stereotypy (e.g. Berkson 1967). For example, McFarland 1966, on displacement activities). Simi- Wood-Gush et al. (1983) found that sows with high larly, endogenous opioids could be the cause of levels of stereotypy showed one-third the explo- stereotypies. Injected opioids will cause or ration of non-stereotypic sows, when presented potentiate stereotyped behaviour (reported by with a novel object, and that this difference was Odberg 1978; reviewed by Robbins & Sahakian maintained whatever the animals were doing 1981), endogenous opioids are involved in general immediately prior to the test. Stereotypies may persistence (e.g. reviewed by Rushen et al. 1990), even be associated with analgesia (e.g. Kravitz et al. and opioids are released at times of stress (Miczek 1960). et al. 1982; Akil et al. 1984). There is one problem Analgesia and physiological signs of coping could with the hypothesis that stereotypy is nothing but be mediated by endogenous opioids (reviewed by the by-product of some other response: it explains Rushen et al. 1990). The association between some why behaviour patterns in general may become stereotypies and opioids has been made on the basis stereotyped in a stressed or aroused animal, but it of work with opiate receptor antagonists such as does not account for the specificity of the patterns naloxone (Cronin et al. 1986b). However, the elicited. hypothesis that stereotypy somehow causes opioid Overall, the data supporting hypotheses con- release would not explain why the abolition of cerning the specific consequences of stereotypy stereotypy by naloxone is immediate (Cronin et al. seems impossible to interpret with certainty. 1985, 1986b; Dodman et al. 1987), rather than There is, finally, evidence supporting the general preceded by a temporary attempt at compensation, 'umbrella' hypothesis that stereotypy, by means as is usually the case in extinction (see e.g. unspecified, is a coping response. This evidence is Richardson & Zaleski 1986). This is also a problem the association between stereotypies and reduced for the hypothesis that the animal superstitiously physiological stress, and reduced negative emotion. associates the behaviour with an opioid release. Examples of correlations between stereotypies A general problem with the evidence considered and physiological signs of coping include some so far is its correlational nature; stereotypies and behaviour patterns of domestic fowl: pacing is 1024 Animal Behaviour, 41, 6

associated with a fall in corticosteroid levels More convincing as evidence that stereotypy is a (Duncan 1970), and head-flicking correlates nega- coping response are the results of a study of stereo- tively with adrenal weight (Bareham 1972, cf. typic jumping in voles (Kennes & de Rycke 1988; Dawkins 1980, page 71 and Odberg 1987a, who Odberg 1989). Stereotypy was selectively prevented misquoted this paper). Cronin (1985) reported that by lowering the cage ceiling. In all animals this young tethered sows often show no stereotypies resulted in raised corticosteroid levels. However, and a chronic rise in corticosteroids; older sows, on the levels were significantly higher and more the other hand, tend to perform stereotypies and sustained in stereotypic than non-stereotypic indi- have no hormonal response. In veal calves there is viduals. The three voles that then developed a new a significant negative relationship between stereo- form of stereotypy had a significantly accelerated typic tongue-playing and the severity of abomasal fall to normal corticosteroid levels. In another lesions (Wiepkema et al. 1984, 1987). Similar re- elegant study, this time of amphetamine-treated sults are found for the type of behaviour patterns rats, the selective pharmacological blocking of the from which some stereotypies may develop. For drug-induced stereotypy was associated with a example, the gastric ulceration developed by rats prolonging of the corticosterone elevation also when forcibly restrained is significantly lower in produced by the stimulant (Jones et al. 1989a). animals that perform the apparently irrelevant dis- Stereotypy is no panacea, however. Some placement activity of biting an object (Vincent et al. stressors, such as cold and inescapable electric 1984). Adjunctive behaviour such as polydipsia shock, seem never to be linked with stereotypy (Brett & Levine 1979; Tazi et al. 1986; Dantzer et al. (Robbins et al. 1990). Furthermore, stereotypy can 1987) and chain-chewing by sows (Dantzer & be reduced or disrupted by very high arousal (e.g. Morm6de 1981) may also be accompanied by Hutt & Hutt 1965; Sahakian & Robbins 1975; physiological signs of coping. reviewed by Robbins & Sahakian 1981), and Behavioural studies have also associated stereo- stressors may sometimes depress, rather than poten- typies with coping, by revealing, for example, tiate, the stereotypies induced by stimulant drugs reduced distress, anxiety or aggression. Children (e.g. Cabib et al. 1985). This is a problem for the performing head-banging stereotypies do not cry arousal-reducing hypothesis (Robbins & Sahakian (Kravitz et al. 1960) and may even enjoy the behav- 1983). Nor is stereotypy always accompanied by iour (Levy 1944); the alarm-calling of frustrated calming or stress-reduction. hens disappears once they develop a high frequency There are several cases where stereotypy does not of stereotyped pacing (Duncan & Wood-Gush seem to result in coping. For example, the biting 1972); and aggressive, frustrated acts decrease in and licking stereotypies of veal calves seem to have frequency as tethered sows' stereotypies develop no influence on abomasal lesions (Wiepkema et al. (Cronin 1985). Schizophrenics and amphetamine 1984, 1987), and chain-manipulation by sows has addicts experience anxiety-reduction and even no influence on the pituitary-adrenal response to an pleasure when performing stereotypies (Fox 1971; aversive extinction condition (Dantzer & Morm6de Rylander 1971, cited by Robbins & Sahakian 1983). Amongst caged bank voles it is the stereo- 1981). Adjunctive or displacement activities, too, typic rather than the non-stereotypic individuals may be associated with behavioural signs of calm- that seem most fearful, tending to flee on exposure ing or reduced distress (Duncan & Wood-Gush to a loud noise (Odberg 1987b). Similarly, adjunc- 1972; Hutchinson 1977). tive polydipsia is not always associated with low- Again, a problem with such data is the interpret- ered corticosteroids (Brett et al. 1982; Jones et al. ation of correlations. Further investigation of the 1989b), and indeed is associated with raised levels association between adjunctive polydipsia and of prolactin (Dantzer et al. 1988). Thus there is no lowered corticosteroids, for example, has revealed predictable relationship between stereotypy, or its the hormones to influence the behaviour, rather source behaviour patterns, and coping. than the other way around (Mittleman et al. 1988; The probable reason for the contradictions in the Levine & Levine 1989). Furthermore, in cases of data is that, as will become evident below, stereo- anxiety-reduction, the effect must be shown to be typies differ in many ways. The properties of one specific to the stereotypy itself, rather than a form of stereotypy are not necessarily those of general result of increased exercise (see Morgan & another. The role of any one stereotypy may also Goldston 1987). depend on the situation in which it is performed. As Mason: Stereotypies reviewed 1025

Falk (1971) pointed out for adjunctive behaviour, a 1989). Candidates for the latter include the form may be maladaptive in one environment, but pituitary-adrenal system (Dawkins 1980, pp. 62- beneficial in another. Thus it may well be that, in 63; Broom 1987); behavioural 'apathy' (Cronin et some cases at least, stereotypy does not have al. 1985; Broom 1987); and the performance of consequences that reward the animal. other behaviour patterns (Broom 1983) such as Unfortunately, evidence that stereotypies have polydipsia (Rushen 1984; Cronin et al. 1985; no function needs as much caution in interpretation Dantzer et al. 1988). If there is equifinality, stereo- as data suggesting that they have. For example, the typies may be readily replaced by other phenomena appropriate measures may not have been made, in some coping animals. This does not mean that especially if beneficial consequences are evident the stereotypy itself has no function. only in the long-term. Alternatively, it may be that there is some threshold effect. For example, if Immediate Reward and Long-term Benefit stereotypy has effects on the animal only if sustained for a certain length of performance, say, Let us suppose that further research does demon- this would obscure the apparent relationship strate that stereotypy has emotional or physiologi- between stereotypy and benefit. Two further prob- cal consequences that appear to benefit the animal. lems are, first, individual differences in 'starting An important question would still remain at issue: point' prior to the development of stereotypy, and, does repeated self-administration of this reward second, that stereotypy may be just one of several benefit the animal in the long-term? Stereotypy means of reaching the same steady state. could be of immediate use only, ultimately unim- There are often considerable differences between portant or even detrimental to the animal's fitness individuals in the extent to which they will respond (Dawkins 1980, page 96; Hinde 1982, page 81). to a situation with stereotypy. This is true of infant So far, evidence for an ultimate function is (Thelen 1979) and institutionalized (Berkson 1967) sparse. For example, Cronin (1985) compared humans, and a number of farm, zoo and laboratory- tethered sows who showed little stereotypy with housed animals (e.g. Draper & Bernstein 1963; those who showed high levels, and found that 'high Staddon & Ayres 1975; Palya & Zacny 1980; stereotypy' sows produced significantly larger Wood-Gush et al. 1983; de Jonge et al. 1986; second and third litters, but smaller fifth and sixth Odberg 1986). If a stereotypy is a coping response, litters. A problem in pursuing this line of investi- the extent to which it is performed will be gation is that fitness is generally estimated as the influenced by the extent to which an animal per- cumulative lifetime reproductive success of an ani- ceives, and is affected by, sub-optimal aspects of the mal (e.g. Trivers 1985). It is not enough to compare environment (Odberg 1987a). For example, indi- animals at just one stage of life, or before the end of viduals may differ in their optimal levels of arousal their reproductive lifespan. In addition there is (Kiley-Worthington 1983; Stevenson 1983; Wood- more to 'reproductive success' than number of sur- Gush et al. 1983), or in the extent to which they can viving offspring: the fecundity of the next gener- predict stressors (Dantzer 1989), or in how frustrat- ations should be assessed too. Other problems ing they find the captive life (Odberg 1986, 1987b). accompany interpretingthe data. For example, a fit Therefore, before assessing the effectiveness of and stereotypic animal may be stereotypic because stereotypy as a coping response by comparing indi- it is fit, rather than the other way round; a poor viduals, one must take into account the animals' animal may not have the energy reserves to allow differing sensitivities to the stereotypy's causal fac- performance of what may be no more than costly tors (Odberg 1987a, 1989). As Rushen (1984) 'comfort' behaviour; and again, the effects of exer- pointed out, it is not clear whether animals that cise in general should be taken into account. In show no stereotypies, for example, are not coping female mink, for example, being lean and muscular or are simply not stressed. improves reproductive success (reviewed by de To understand the role of stereotypy, one must Jonge et al. 1986). also realise that individuals may take alternative routes to the same end point. This is the problem of Conclusion equifinality (Bateson 1976). Therefore, in the case of stereotypy, one must assess the use of alternative Stereotypies are defined as being without coping mechanisms (Broom 1985; 0dberg 1987a, obvious goal or function, but closer study suggests 1026 Animal Behaviour, 41, 6 that they could be reinforced and that they might be The first problem is that authors differ as to just used to ameliorate a sub-optimal environment. how rigid or repetitive a behaviour pattern has to be However, although intriguing, this evidence is not before they will call it a stereotypy. Because stereo- always strong. Persistence may be explained by typies become progressively more stereotyped with processes other than reinforcement, and much of repetition, speed of performance and arousal, there the evidence for coping is based on correlations is no rigid dividing line between what is 'truly' rather than an understanding of underlying mech- stereotypic and what is not; a continuum exists (for anisms. Clearer results might be obtained by a similar problem see Hinde 1970, page 21; and accurately recording the relative time-courses of Dawkins 1986 on 'fixed action patterns'). the behaviour and the relevant physiological par- This continuum is reflected in a range of vari- ameters, and by further experiments in which ations on the basic definition ofstereotypy. Dantzer stereotypy levels are selectively manipulated. (1986) reserved the term for fixed sequences of Investigation of the factors that predispose behaviour, and Kiley-Worthington (1977) defined individuals to stereotypy may also help in our stereotypy as 'fixed in all details', a very restrictive understanding of this behaviour. definition if by this she means fixed in location Even if stereotypies are coping mechanisms in and timing as well as morphology. In contrast, the short term, it would remain to be seen whether Forrester's (1980) stereotypies are not completely they are associated with long-term benefit, such as inflexible, and Fraser & Broom (Broom 1983; improved fitness. Nor would it mean that we can be Fraser & Broom 1990) define a stereotypy as being complacent about the welfare of stereotypic ani- only 'relatively' invariant. Tics and mannerisms are mals. This is for two reasons. First, the likelihood is sometimes called 'stereotypies' in human psychi- that the animal has been in an aversive situation in atric literature (reported by (}dberg 1984a), and to the past. Second, it remains an open question confuse the picture further, Berkson and co-workers whether an animal that spends a lot of time in a (1963; Berkson 1967) even described some behav- stereotypy really is better off than one that, say, iour patterns, such as abnormal limb-postures and develops a gastric ulcer (Wiepkema 1987). The ani- eye-poking, as 'non-repetitive stereotypies'. mal's welfare, if defined in terms of the amount of A consequence of this confusion is that studies coping it is having to do (Broom 1986; Fraser & often differ in the ways in which they classify behav- Broom 1990), could be said still to be poor. iour. There may even be differences within the work of the same authors. Odberg (1989) pointed out that Dantzer & Morm6de (1981, 1983) described S T E R E O T Y P I E S ARE chain-chewing as a stereotypy in one paper, and an H E T E R O G E N E O U S adjunctive behaviour in another. De Jonge et al. (1986), in their studies of farmed mink, chose to So far, I have emphasized the similarities between divide repetitive, apparently purposeless loco- different forms of stereotypy and discussed them as motion into two categories, only one of which, on a group. However, there are two important con- the basis of its greater rigidity and persistence, did siderations when discussing the biological signifi- they call 'stereotypy'. However, when I observed cance of stereotypies. First, are stereotypies mink I found this classification over simple, exclud- unambiguously identifiable in practice? And ing complex patterns even when highly predictable. second, are they really equivalent in source of origin, One way around the problem of detecting repeti- mode of development and potential function? I tiveness in complex behaviour, which might other- discuss each of these points in turn. wise not be classed as stereotyped, is to use informational redundancy to quantify the rep- etition within behavioural sequences (Stolba et al. Identifying Stereotypies 1983). Stereotypies are not, unfortunately, unam- The morphological criteria used in identifying a biguous to identify. There are two main problems: 'genuine' stereotypy is not the only problem. The the morphological criteria used in identifying a second major problem is that stereotypies are stereotypy, and the problem of distinguishing a defined as being without obvious function. How- behaviour pattern with a function from one ever, when stereotypies are exaggerated forms of without. normal behaviour (Kiley-Worthington 1977), it is Mason." Stereotypies reviewed 1027 difficult to say at what point they stop being adapt- developmental or functional significance, and ive. For example, are the body-rocking and thumb- hence of particular importance when assessing the sucking, shown by normal primates at a certain equivalence of different forms. stage of infancy (Berkson 1967; Thelen 1979), examples of stereotypy? Hutt & Hutt (1965) Deprivation and cage stereotypies showed that, when familiar with a new toy, the stereotypy of autistic children would decrease, with Deprivation stereotypies appear in animals that a concomitant rise in play. However, as Robbins & have been socially isolated or subjected to sensory Sahakian (1981) point out, the play was not nor- deprivation since birth or infancy (Draper & mal; it involved stereotyped, repetitive patterns of Bernstein 1963; Berkson 1967; Ridley & Baker movement, and perhaps could have been classified 1982). These include institutionalized children (e.g. as a stereotypy itself. The close parallels between Mason & Green 1962). They may also appear in headshakes in jungle-fowl, Gallus gallus spadiceus, animals chronically deprived of the opportunity to and those made by intensively housed hens, along perform specific behaviour patterns, for example in with their possible role in attentional mechanisms, buntings prevented from making the intention suggest that the behaviour might have a function movements of flight by a low cage ceiling (Andrew when shown 'occasionally', but perhaps should be 1956, cited in Hinde 1970). They tend to be non- regarded as a stereotypy when shown 'often' locomotory, and may involve self-mutilation. They (Fraser & Broom 1990). A similar problem was are exacerbated by amphetamines (e.g. Berkson & considered by Rushen et al. (t990). They chose not Mason 1964; Fitz-Gerald 1967, cited in Lyon & to call post-food rooting a stereotypy, even though Robbins 1975). They are very difficult to disrupt repetitive and seemingly unconsummatory, because (Ridley & Baker 1982), and may persist even when it closely resembles the normal post-feeding behav- the animal is put into a normal environment (e.g. iour of free-living pigs. This was even though, in Davenport & Menzel 1963; Meyer-Holzapfel 1968). some individuals, the rooting appeared unusually Cage stereotypies, in contrast (Draper & persistent. As they conclude, 'which behaviours to Bernstein 1963; Berkson 1967; Ridley & Baker include as "stereotypies" is not a simple issue'. 1982), tend to be locomotory, and are not increased (Odberg 1984b), indeed are sometimes abolished (Ridley & Baker 1982), by amphetamines. They are The Equivalence of Stereotypies typical of small or barren cages, but can be altered There are many differences between stereotypies. by changes in the environment. Ridley & Baker They are heterogeneous in form and rigidity, tem- (1982) suggested that they are the response of a poral organization, eliciting stimuli, and degree of normal central nervous system to a sub-optimal variability between individuals. They are also environment. heterogeneous in ontogeny: stereotypies are derived This scheme is not without its problems. For from a range of source behaviour patterns, and example, the division between deprivation and cage probably represent a range of motivational states stereotypy is not always clearcut in practice, (Dawkins 1980; Duncan & Dawkins 1983). probably because the effects of caging are more In an effort to clarify the situation various profound on a young than on a mature animal attempts have been made to classify stereotypies. (Berkson 1968), and cage environments are often Distinctions have been drawn between the follow- likely to involve a degree of sensory deprivation. ing types: (1) deprivation and cage; (2) terminal and Self-mutilation is not unique to monkeys with a interim; (3) abbreviated and non-abbreviated; (4) deprived infancy (Erwin & Deni 1979; Ridley & developing and established; and (5) stimulant- Baker 1982), and other stereotypies that seem to be induced and environment-induced. of the irreversible, 'deprivation' type can be These schemes overlap, and the distinctions they produced in animals that are adult rather than make between different forms may in some cases be young at the time of treatment, as Andrew's work artificial. However, I examine each in some detail. with buntings (ibid.) and Hinde (1958) have shown. This is partly to discuss the limitations of each Conversely, deprivation stereotypies are not scheme, partly to emphasize the many differences always irreversible; deprived rhesus monkeys have between stereotypies, and partly to highlight the been cured through the use of infant 'therapists' features of stereotypies that may be of particular (e.g. Harlow & Suomi 1971), and the stereotypies of 1028 Animal Behaviour, 41, 6 isolation-reared chimpanzee_s are reduced, at least Stereotypy is not only organized in this way in in the short-term, by the provision of objects to the laboratory. In farmed mink (de Jonge et al. manipulate (Berkson et al. 1963). 1986; de Jonge & Carlstead 1987) and some zoo Another similarity blurs the division between the animals (e.g. Odberg 1984a), pacing reaches a two categories: both increase with arousal (Berkson maximum just before feeding. Pigs root (Dantzer & & Mason 1964). For example, both are exhibited in Morm~de 1982; Cronin 1985), bar-bite and head- response to a novel environment (Mason & Green weave (Dantzer & Mormrde 1982; Rushen 1984, 1962; Berkson & Mason 1964) and increase in small 1985; Cronin 1985) predominantly in the pre- cages (Draper & Bernstein 1963). This could feeding period, while most of their stereotypy, in suggest some common mechanisms (Berkson the form of sham-chewing (Dantzer & Mormede 1967). 1982; Rushen 1984, 1985; Cronin 1985), chain- Finally, the scheme is a little simplistic. Some manipulation (Dantzer & Mormrde 1982), drinker- cage stereotypies are elicited by one aspect of the playing and polydipsia (Rushen 1984) peaks after environment, others by another. For example, feeding. Keiper (1969) found some stereotypies in canaries, There are some problems with this classification, Serinus canaria, to be abolished by enlarging the however. Again, not all stereotypies fit readily into cage, others by increasing the foraging necessary to one or other class. For example, the interim run- obtain food. Similarly, the cage stereotypies ning behaviour of one intermittently fed rat produced by a schedule of fixed feeding are of at appeared to have such 'momentum' that its persist- least two different types (see Terminal and interim ence left no time for a terminal response (Staddon stereotypies). Deprivation stereotypies are also & Ayres 1975). Sow drinker-pressing and manipu- heterogeneous. For exmple, some mental defectives lation (Broom & Potter 1984; Rushen et al. 1990), show mainly rhythmic body movements, others, chain-playing (Rushen 1984; Rushen et al. 1990) complex hand movements. Both are associated and vacuum chewing (Rushen 1984, 1985), and the with. lowered reactivity to external stimuli. How- stereotypies of captive mink (de Jonge et al. 1986) ever, in the former, responsiveness is generally can be shown by animals at all times of day, in both higher than in individuals who show no stereotypy; terminal and interim periods. Neither are stereo- in the latter, responsiveness remains low even when typies restricted to the interval between inter- the individual is not actively engaged in the mittent stimuli: some may occur during stimulus behaviour (Berkson 1967). presentation, e.g. pigeons pecking during an elec- tric shock (Sterritt 1962, cited in Hinde 1970, page Terminal and interim stereotypies 208); and stereotypies occur in animals that are On a regime of periodic feeding, stereotypies not on a schedule at all (e.g. Keiper 1969; Odberg develop both as the time of food delivery approaches 1986). and during the period after feeding. From their Furthermore, one cannot assume that within timing within the inter-food interval, these are called each category a~l stereotypies are equivalent. For 'terminal' and 'interim' stereotypies, respectively example, Anderson & Shettleworth (1977) found (Staddon & Simmelhag 1971). that when the expected food did not arrive, the vari- Interim behaviour is the more idiosyncratic and ous interim patterns of hamsters, Mesocricetus may represent adjunctive behaviour (Staddon & auratus, changed in different ways. Similarly, some Simmelhag 1971; Rushen 1984), escape attempts animals have initial, temporary idiosyncrasies of (Staddon & Simmelhag 1971), or be due to disinhi- terminal stereotypy, which then change to the bition (Anderson & Shettleworth 1977). Terminal species-typical form (Staddon & Simmelhag 1971), behaviour, in contrast, is subject to little or no indi- and it could be that these differ from the latter in vidual variation on a given regime, and when the being superstitious. Also, the terminal patterns reinforcer is food it appears related to appetitive seen when the regular stimulus is aversive, e.g. an behaviour (Staddon & Simmelhag 1971; Anderson electric shock (Hutchinson 1977), is presumably & Shettleworth 1977). The behaviour's lack ofidio- not equivalent to those seen during intermittent syncracy, and occurrence even if it reduces the rate food reward. Even within schedules using the same of food-delivery by interfering with an operant reinforcer (food), there are disagreements as to response, suggests that it is not merely superstitious what is represented by the stereotypies. For (Staddon & Simmelhag 1971). example, it may be the interim rather than the Mason: Stereotypies reviewed 1029 terminal stereotypies that develop from appetitive chimpanzees to have no normal equivalent, but behaviour (Palya & Zacny 1980; Rushen 1984). Mason & Green (1962) suggested that rocking, Rushen (1984, 1985) suggested that, in sows, pre- especially when accompanied by self-clasping, feeding (terminal) stereotypies represent frus- mimics the way that an infant rocks and rubs up tration. Interpretation may depend on the species against its mother when distressed. Similarly, self- under study. biting may have an equivalent in play-fighting, stereotypies with the hands may originate in the normal hand movements of infant monkeys, and so Abbreviated and non-abbreviated stereotypies on. However, detailed longitudinal studies would Some stereotypies closely resemble normal be necessary to establish homology reliably behaviour in form. Examples include pacing (Berkson 1967). (Morris 1964; Broom 1983), and self-sucking in Furthermore, not all stereotypies fit neatly into infant primates (Berkson 1967). Other stereotypies this scheme. For example, sow stereotypies grow differ from their original source behaviour in that longer with continued restraint, new components they have lost elements of the original action being added (Cronin et al. 1984). Similarly, the pattern. Such stereotypies are sometimes known complexity of mink stereotypies increases with age as 'incomplete' (van Putten 1982; Broom 1983). (de Jonge et al. 1986). In some cases this may be The distinction between abbreviated and non- the result of increased maturity and muscular abbreviated forms of stereotypy is discussed for coordination (Bernstein & Mason 1962). Also, a two reasons. First, it has been contended that a stereotypy may become more, rather than less, behaviour pattern that appears 'complete', i.e. to environment-directed with age. For example, head- have an equivalent pattern in the animal's normal banging may develop in infants who previously had behavioural repertoire, should never be called a shown head-rolling or body-swaying (Kravitz et al. stereotypy (van Putten 1982), even though 1960). Nor is abbreviation exclusively the side- invariant and of no apparent function. Second, effect of long-term repetition; a stereotypy may also the process of abbreviation may have functional simplify if causal factors are less intense. For significance. example, the somersaulting of one rhesus monkey Dantzer (1986) suggested that the loss of was reduced to mere hints in a larger cage (Draper elements might be responsible for the transition & Bernstein 1963). between environment-directed stereotypies, such as bar-biting, and the self-directed stereotypies, such Developing and established stereotypies as sham-chewing, more common in older sows. A similar change can be seen in horse stereotypies, There are qualitative differences between devel- crib-chewing sometimes progressing to air-sucking oping and established stereotypies in the following (Fraser 1980). Dantzer attributed no functional sig- respects: in the apparent emotional, motivational nificance to this transition, explaining it in terms of correlates of the behaviour; in the neural substrates repetition and rapidity of performance. Cronin involved; in the fixity of performance; and in the (1985), in contrast, suggested that the frustrations degree to which the stereotypies are emancipated of being restrained, prompt environment-directed from their original eliciting stimuli (Duncan stereotypies. He suggested that these are derived & Wood-Gush 1974; Kiley-Worthington 1977; from redirected aggressive behaviour, the younger t)dberg 1978). sows, with less experience of tethering, finding Developing stereotypies are inhibited by tran- restraint the most stressful. Self-directed activities, quillizers (Feldman & Green 1967; Duncan & such as oral stereotypies, are more common when Wood-Gush 1974), which could suggest that their all is quiet on the farm, and in the older, more ex- elicitation depends on emotional, limbic systems perienced sows. They may represent some kind of (e.g. reported by Kennes & Odberg 1987; Odberg compensatory self-stimulation. 1989). Tranquillizers had no effect on these stereo- One problem with this classification is that typies once fully established (Feldman & Green authors can differ in what they consider has an 1967; Duncan & Wood-Gush 1974), leading equivalent in the normal behavioural repertoire. to suggestions that established stereotypies are For example, Berkson & Mason (1964) considered emotionally neutral (e.g. Duncan & Wood-Gush the rocking and swaying of deprivation-reared 1974), 'pure motor automatisms' (Kennes & 1030 Animal Behaviour, 41, 6

Odberg 1987; 0dberg 1989). Kennes et al. (1988) account for the failure of some stereotypies to found that the opiate receptor antagonist naloxone fit neatly into the terminal/interim classification, did not inhibit stereotypies in bank voles over a and perhaps for the differences in how authors certain age. Cronin et al. (1985, 1986b) have also describe the distribution of, for example, drinker- found an inverse relationship between age of manipulation by sows (see Terminal and interim stereotypy and the latency with which it was sup- stereotypies). Kiley-Worthington (1977) suggested pressed by naloxone, in sows. It has been hypoth- that the developmental change in the nature of a esized that stereotypies depend on brain opioids stereotypy explains the discrepancy between the in their early stages (e.g. Kennes et al. 1988). results of Levy (1944) and Hutt & Hutt (1965). Established stereotypies, however, seem to be Environmental complexity, in the former study, essentially under dopaminergic control (Cronin et increased the stereotypy shown by autistic children, al. 1985; Kennes et al. 1988). while in the latter study, it decreased performance Established stereotypies also differ from devel- in children whose stereotypies were not so well oping ones in being much more difficult to discour- established. The difference between developing and age or interrupt (Kiley-Worthington 1977; Cronin fully developed stereotypies may also explain the et al. 1984). For example, once firmly established, confusing relationship between stereotypy and lit- the pacing shown by food-deprived hens faced with ter size in sows of different ages (Cronin 1985); why a covered food-dish does not disappear even when Cronin (1985) found that, in contrast to the results food is made available (Duncan & Wood-Gush of Wood-Gush et al. (1983), sows with high levels of 1972). Established stereotypies may even be facili- stereotypy were more attentive to external stimuli tated by stimuli that would have interrupted them and faster to react than sows with low levels; and earlier in their development (Fentress 1977). why barbiturates reduced the deprivation stereo- Furthermore, they are performed outside the orig- typies of chimpanzees in one study (Fitz-Gerald inal eliciting situation (Odberg 1978), sometimes 1964, cited in Berkson 1967), but not those of even in the absence of any apparent conflict mentally handicapped humans in another (Berkson (Kennes et al. 1988). 1967). It is unclear whether the changes involved in this transition occur synchronously (Kennes et al. Stimulant-induced and en vironment-induced 1988). It is possible that the change in emotional stereotypies involvement does not coincide with emancipation: Cronin et al. (1984, 1985) described the post-feeding Stereotypies are induced by psychomotor stimu- stereotypies of tethered sows as changing from lant drugs such as amphetamine and apomorphine short bursts of apparently aggressive activity to (Lyon & Robbins 1975; Robbins & Sahakian prolonged bouts of much less aggressive behaviour. 1981). The stereotypy develops from behaviour Only if restraint continued did this behaviour come that was predominant prior to treatment, for to be performed at all times of day. Nor is it clear example from eating in hungry animals (Ellinwood exactly how this categorization overlaps with & Kilbey 1975; Robbins 1982; Dantzer 1986; the schemes classifying stereotypy as complete/ reviewed by Robbins et al. 1990). It is usually idio- incomplete, or abbreviated/non-abbreviated. Also, syncratic (e.g. Sahakian & Robbins 1975) and an note that one individual may perform both devel- individual's characteristic stereotypy will be shown oping and established forms of stereotypy. For on successive amphetamine trials even if these are example, Dodman et al. (1987) found that opiate months apart (Lyon & Robbins 1975). Locomotor receptor antagonists abolished crib-chewing in activity also increases on treatment with a stimu- horses, but did not affect their weaving. lant, and this is also stereotyped in a sense, the ani- Although probably a spectrum rather than a mal following a limited number of fixed routes dichotomy, it would appear that the distinction (Robbins & Sahakian 1981). There is also a corre- between developing and established stereotypies is sponding stereotypy of routine and thought similar valid and important, and might help to explain why to that of schizophrenics (Robbins 1976; Robbins different studies sometimes yield contradictory & Sahakian 1981; Ridley & Baker 1982). There is results. For example, the emancipation of stereo- some disagreement as to what the drug-induced typy from its original post-meal context, as stereotypies represent. As already mentioned, some described by Cronin et al. (1984, 1985), would believe they are the functionless side-effects of over- Mason: Stereotypies reviewed 1031 stimulation (Lyon & Robbins 1975; Robbins 1982), intense stimuli can interfere with environment- while others present evidence that they are induced stereotypy (Fentress 1977; Robbins & associated with coping (Jones et al. 1989a). Sahakian 1981). Stereotypy becomes more intense with increasing The involvement of isolated limbs is further remi- doses of stimulant (e.g. Lyon & Robbins 1975), and niscent of the deprivation type of environment- with repetition of the treatment, the animal becom- induced stereotypy. Stimulant drugs may even ing sensitized to the drug (e.g. Robbins & Sahakian increase the preformance of an animal's existing 1981). As the stereotypy intensifies, the movements deprivation stereotypies (e.g. Berkson & Mason become more and more dissociated from their orig- 1964; Fitz-Gerald 1967, cited in Lyon & Robbins inal context, in timing and in orientation (Robbins 1975), as discussed earlier. However, other, cage- 1976, 1982; Robbins & Sahakian 1981). Rate of type, forms of environment-induced stereotypy are repetition increases, the movements become not enhanced by the administration of stimulants increasingly abbreviated, and the stereotypy (e.g. Odberg 1984b). becomes species-typical instead of idiosyncratic A final important point is that, like stereotypies (e.g. as reviewed by Lyon & Robbins 1975). It typi- induced by the environment, stimulant-stereotypies cally involves oro-facial movements, or isolated are a heterogeneous group. Different drugs result in limbs (e.g. Robbins & Sahakian 1981), but at stereotypies that differ in typical appearance extreme doses the animal can do little more than (reviewed by Robbins & Sahakian 1981), response twitch. to a dose increase (Fray et al. 1980), and the way This transition perhaps parallels the simplifi- in which they are affected by, for example, food- cation seen during the development of other forms deprivation (see e.g. MacLennan & Maier 1983). of stereotyped behaviour (Dantzer 1986). Drug- They may also involve opioid systems to different induced behaviour has further similarities with extents (see Robbins & Sahakian 1981). Further- environment-induced stereotypy. For example, it more, the various stereotypies elicited by increased seems very compulsive and will persist even when or repeated dosage of one drug show different pat- punished (Lyon & Robbins 1975; Robbins & terns of sensitization (Eichler et al. 1980), and may, Sahakian 1981). Robbins & Sahakian (1981) as they change from complex to more simple forms, suggested that the subject may have restricted have different neurophysiological bases (reviewed attention. Dopaminergic systems are involved by Robbins & Sahakian 1981, 1983; see also (Robbins & Sahakian 1981), as they are in some Mittleman et al. 1986). environment stereotypies (0dberg 1984b; Kennes et al. 1988). In addition, the involvement of opioids Conclusion in some cases (opiate receptor antagonists block the Stereotypy is not a category with a clearly stereotyped gnawing produced by apomorphine, defined border: the stereotypies described by some although they appear to have no effect on ampheta- authors may be classed differently by others. Nor mine stereotypies; Robbins & Sahakian 1981) does the term apply to a group of behaviour pat- parallels the involvement of opioids in some terns that are homogeneous: there are many differ- environment-induced stereotypies. A further simi- ences between the various forms of stereotypy. larity between drug- and environment-induced Their stereotyped nature would not seem reason stereotypies is the effect of stress, which often enough for assuming genuine equivalence, since a potentiates the behaviour. shared repetitive rigidity in no way implies that the In general, stressors sensitize animals to the behaviour patterns also share a common cause, stereotypy-inducing effects of stimulants (as goal or function; nor does the other characteristic reviewed above) and seem to interact with the drug of stereotypies, their lack of apparent function, for in an additive way (Robbins et al. 1990). The stimu- it is hardly biologically meaningful to group things lants may be acting as stressors themselves (e.g. on the basis of what we do not know about them. Mittleman et al. 1986). In some cases stressful treat- ments do not enhance the development of stereo- G E N E R A L C O N C L U S I O N S typy, and may even inhibit or disrupt it (Sahakian & Robbins 1975; and e.g. Lyon & Randrup 1972, Stereotypies have some linking characteristics, but cited in Robbins & Sahakian 1981; and Cabib et al. they differ in many others. Furthermore, their com- 1985). This may be similar to the way in which very mon features may be trivial. It is therefore not 1032 Animal Behaviour, 41, 6 reasonable to assume that all stereotypies are McCune, Mike Mendl, Frank Odberg, Trevor homogeneous. This should be taken into account Robbins, Jeff Rushen, Michael Simpson and Nigel when discussing their welfare implications or func- Warburton for invaluable discussion and com- tional significance. Arousal reduction, say, or ments. I was supported by a SERC Postgraduate lowered responsiveness, could be associated with Studentship. one stereotypy but not with another, even within the same individual (Lovaas et al. 1971; Cronin & Wiepkema 1984; Odberg 1987), and a behaviour R E F E R E N C E S pattern might have a function in one context (Falk Akil, H., Watson, S. J., Young, E., Lewis, M. E., 1971), or at one stage of development (see Dantzer Khachaturian, H. & Walker, J. M. 1984. Endogenous 1989, on adjunctive polydipsia), but not in another. opioids: biology and function. A. Rev. Neurosci., 7, Because of this heterogeneity, care must be taken 223-255. not to extrapolate without reason from one animal Anderson, J. R. & Chamove, A. S. 1984. Allowing captive primates to forage. In: Standards in Laboratory or from one situation to another. 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