Georgia Mason

Stereotypies: a critical review

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, becoming more readily elicited by a wider range of circumstances. Therefore the properties of one stereotypy are not necessarily those of another.

Dissociation in the effects of neonatal maternal separations on maternal care and the offspring's HPA and fear responses in rats

The development of the hypothalamic–pituitary–adrenal (HPA) response to stress is influenced by the early mother–infant relationship. In rats, early handling (brief daily mother–offspring separations) attenuates the adult offsprings HPA and fear responses compared to both nonhandling (no separations) and maternal separation (prolonged daily separations). It has been proposed that variation in the amount of maternal care mediates these effects of neonatal manipulations on the adult offsprings stress and fear responses. Here we tested this hypothesis by assessing maternal care and the adult offsprings HPA and fear responses in Lister hooded rats which were subjected to either early handling (EH) or maternal separation (MS) from postnatal day 1–13, or were left completely undisturbed (nonhandled, NH) throughout this period. Both EH and MS induced a more active nursing style and elevated levels of maternal care compared to NH. Total levels of maternal care were indistinguishable between EH and MS, but diurnal distribution differed. MS dams showed elevated levels of maternal care following the 4‐h separation period, thereby fully compensating for the amount of maternal care provided by EH dams during the time MS dams were separated from their pups. However, while EH resulted in reduced HPA and fear responses in the adult offspring compared to NH, MS and NH offspring did not differ. Our findings therefore demonstrate dissociation in the effects of EH and MS on maternal care and on the stress and fear responses in the offspring. This indicates that maternal care cannot be the sole mediator of these effects.

Frustrations of fur-farmed mink

Mink may thrive in captivity but they miss having water to romp about in.

Evidence for a relationship between cage stereotypies and behavioural disinhibition in laboratory rodents.

Cage stereotypies-abnormal, repetitive, unvarying and apparently functionless behaviours-are common in many captive animals, sometimes resulting in self-injury or decreased reproductive success. However, a general mechanistic or neurophysiological understanding of cage stereotypies has proved elusive. In contrast, stereotypies in human mental disorder, or those induced by drugs or brain lesions, are well understood, and are thought to result from the disinhibition of behavioural selection by the basal ganglia. In this study, we found that the cage stereotypies of captive bank voles also correlate with signs of altered response selection by the basal ganglia. Stereotypic bar-mouthing in the caged voles correlated with inappropriate responding in extinction learning, impairments of response timing, evidence of a knowledge-action dissociation, increased rates of behavioural activation, and hyperactivity. Furthermore, all these signs intercorrelated, implicating a single underlying deficit consistent with striatal disinhibition of response selection. Bar-mouthing thus appears fundamentally similar to the stereotypies of autists, schizophrenics, and subjects treated with amphetamine or basal ganglial lesions. These results represent the first evidence for a neural substrate of cage stereotypy. They also suggest that stereotypic animals may experience novel forms of psychological distress, and that stereotypy might well represent a potential confound in many behavioural experiments.

A demanding task: using economic techniques to assess animal priorities.

Copyright 1998 The Association for the Study of Animal Behaviour.

Do the stereotypies of pigs, chickens and mink reflect adaptive species differences in the control of foraging?

Abstract The food-related stereotypies of some captive species (e.g. mink) are performed most often prior to feeding, while those of others (e.g. pigs and chickens) occur at low levels before feeding and increase after food consumption. It has been suggested that these differences reflect adaptive species differences in how feeding behaviour is controlled. However, this hypothesis rests on several underlying assumptions for which there is incomplete support. One assumption is that there are indeed species differences in the design of motivational systems, and we suggest some specific predictions to test this idea. For example, the ingestion of small portions of food should lead to greater enhancement of local searching behaviour in species whose food supply is particulate and patchy. The basic premise underlying this evolutionary explanation for species differences in stereotypy is that such differences are genetically based, not an artefact of the way different animals are kept. However, we argue that variation in husbandry may also cause variation in stereotypies. For example, the autoshaping literature reveals factors likely to affect pre-feeding stereotypies: unreliable predictors of food delivery, or predictors that occur some time before food is presented, give rise to general locomotory search phases of appetitive behaviour rather than behaviour related to food handling. Farmed mink may therefore show high levels of pre-feeding locomotor behaviour principally because sounds predicting the delivery of their daily meal are quite unreliable and commence long before the food arrives. Lack of space may also inhibit locomotor forms of pre-feeding stereotypies in pigs and chickens. In addition, the high post-feeding appetitive behaviour of these two species may be caused by lack of satiation following food. Overall, evolutionary hypotheses make predictions about stereotypy based on feeding ecology, but there are also alternative causal hypotheses that make predictions based on aspects of husbandry. Together, these may help to explain the forms of existing stereotypies, and to anticipate the forms likely to arise in new husbandry systems or in newly captive species.

Frustration and perseveration in stereotypic captive animals: is a taste of enrichment worse than none at all?

Stereotypic behaviours are common in animals in impoverished housing, arising from two complementary processes: (1) thwarted attempts to perform motivated behaviours; (2) forebrain dysfunction impeding normal behavioural inhibition. When enriched animals are moved to impoverished housing, they are sometimes protected against developing stereotypic behaviour, but in other cases become even more stereotypic than animals housed lifelong without enrichment. Negative contrast-induced frustration must occur in both scenarios. We hypothesise that sustained behavioural responses to this frustration are prevented in the former by normalised forebrain function, but exacerbated in the latter by forebrain dysfunction. ICRCD-1 mice reared in enriched or standard cages were re-caged at 3 months to standard conditions. Here, previously-enriched mice became far more stereotypic than mice reared from birth in such conditions. To investigate the role of frustration, we assessed both corticosterone output and motivation (break-point) to regain enrichments. We also assessed perseveration via extinction learning. As predicted, previously-enriched mice were as perseverative as standard-raised mice, and frustration seemed to play a causal role in their exacerbated stereotypic behaviour. Previously-enriched mice showed higher motivations to access enrichments, and only in this group did these correlate with corticosterone levels after re-caging; furthermore only in previously-enriched mice did corticosterone responses to re-caging predict stereotypic behaviour 30 days later (males only). All results need replicating and further investigation. However, they suggest for the first time that individual risk factors related to the HPA axis predict stereotypic behaviour following enrichment-removal, and that previously-enriched mice have lasting motivational differences from standard-raised mice, suggesting sustained behavioural effects related to the frustration of enrichment-loss.

What’s in a peck? Using fixed action pattern morphology to identify the motivational basis of abnormal feather-pecking behaviour.

Like many captive animals, hens, Gallus gallus, used for agricultural production perform abnormal behaviours. They are particularly prone to feather pecking, the severest form of which involves the pecking at and removal of feathers, which can cause bleeding and even stimulate cannibalism. The two main hypothesized explanations for feather pecking concern frustrated motivations to forage or, alternatively, to dustbathe, leading to redirected behaviour in the form of pecks at plumage. Previous work on pigeons has shown that the detailed morphology of pecks involved in drinking and feeding, or in working for food or water, involves motivationally distinct ‘fixed action patterns’. We therefore used methods similar to these fixed action pattern studies to quantify the motor patterns involved in foraging and in dustbathing pecks, for comparison to feather pecking. We videoed 60 chickens pecking at a variety of forages and dustbaths, along with novel objects, water and bird models that could be feather pecked. We recorded the durations of the head fixation before the peck, between the head fixation to beak contact with each stimulus and of the whole peck sequence. We used mixed models to assess whether the motivation underlying a peck affected its morphology and whether severe feather pecks resembled or differed from either dustbath or foraging pecks (or even novel-object pecking or drinking). The motor patterns involved in pecks at forages, dustbaths, novel objects and water all varied significantly; importantly, the motor patterns involved in pecking during dustbathing and foraging differed (P 0.95) but different from all other pecks, including dustbathing (P < 0.0001 for all measures). These results indicate that severe feather pecking derives from frustrated motivations to forage, not to dustbathe. More broadly, they suggest that finely analysing fixed action pattern morphology can help elucidate the motivational bases of puzzling abnormal behaviours in captive animals.

Long-term effects of cage-cleaning frequency and bedding type on laboratory rat health, welfare, and handleability: a cross-laboratory study

Cage-cleaning is necessary for a hygienic environment, but since rats communicate using scent, they might suffer if their cages are cleaned too frequently. Male rats (Sprague–Dawley and Wistar) were kept for five months across four animal units. Their cages were cleaned twice-weekly, weekly, or every two weeks, and contained either aspen woodchips or absorbent paper bedding. Aggression, injuries and general health, weight gain, chromodacryorrhoea (a stress-related Harderian gland secretion), handleability, and lung pathology were monitored, as was in-cage ammonia. Cleaning frequency had no clear impact on rat welfare, although frequent cleaning decreased ammonia concentrations and handleability, and non-aggressive skirmishing was highest in weekly cleaned rats. Surprisingly, bedding type did not affect ammonia, but all ammonia readings were unexpectedly low. However, rats kept on aspen had greater sneezing rates and lung pathology than those on paper bedding, but also had higher body weights. The results raise concerns about aspen bedding, which is relatively inert compared with other wood beddings, but nevertheless more harmful than paper. Animal unit significantly affected eight of the 11 variables tested, having interactive effects on five of them. The study also demonstrates the interactive effects of different animal units, casting doubt on the feasibility of standardization. We explored multiple variables of interest, so all findings require confirmation through further work. Nevertheless, cage-cleaning rates seem to affect socially housed male rats little, while bedding type has important effects on rat health.

Environmental Enrichment Reduces Signs of Boredom in Caged Mink

Animals housed in impoverished cages are often labelled ‘bored’. They have also been called ‘apathetic’ or ‘depressed’, particularly when profoundly inactive. However, these terms are rarely operationally defined and validated. As a negative state caused by under-stimulation, boredom should increase interest in stimuli of all kinds. Apathy (lack of interest), by contrast, should manifest as decreased interest in all stimuli, while anhedonia (loss of pleasure, a depressive symptom) should specifically decrease interest in normally rewarding stimuli. We tested the hypotheses that mink, a model carnivore, experience more boredom, depression-like apathy, or anhedonia in non-enriched (NE) cages than in complex, enriched (E) cages. We exposed 29 subjects (13 E, 16 NE) to ten stimuli categorized a priori as aversive (e.g. air puffs), rewarding (e.g. evoking chasing) or ambiguous/neutral (e.g. candles). Interest in stimuli was assessed via latencies to contact, contact durations, and durations oriented to stimuli. NE mink contacted all stimuli faster (P = 0.003) than E mink, and spent longer oriented to/in contact with them, albeit only significantly so for ambiguous ones (treatment*type P<0.013). With stimulus category removed from statistical models, interest in all stimuli was consistently higher among NE mink (P<0.0001 for all measures). NE mink also consumed more food rewards (P = 0.037). Finally, we investigated whether lying down while awake and stereotypic behaviour (both increased by NE housing) predicted these responses. Lying awake positively co-varied with certain measures of increased exploration. In contrast, stereotypic ‘scrabbling’ or locomotion (e.g. pacing) did not. Overall, NE mink showed no evidence of apathy or depression, but instead a heightened investigation of diverse stimuli consistent with boredom. This state was potentially indicated by spending much time lying still but awake (although this result requires replication). Boredom can thus be operationalized and assessed empirically in non-human animals. It can also be reduced by environmental enrichment.