Social reinstatement responses of meat-type chickens to familiar and unfamiliar conspecifics after exposure to an acute stressor

Runway tests are considered indicative of underlying sociality in birds and their ability to make social discriminations. We evaluated whether experience of a prior stressor alters the subsequent affiliation responses of 9 or 10-day-old chicks simultaneously exposed to familiar (cagemates) and unfamiliar conspecifics placed in goal boxes at opposite ends of a runway. Birds were housed in groups of eight in home cages. Half of the birds in each home cage were used as either familiar or unfamiliar social stimuli in the goal boxes. The other half of the birds were randomly assigned either to a control (CON; n = 51) group that remained undisturbed until testing or to a stress-treatment (STR; n = 52) group that was exposed to a 5-min restraint stressor, returned to its home cage and then tested 1 h later. Birds were individually tested in the runway for 5 min and the behaviours video-recorded. During revision of tapes, the projected floor image of the runway was divided into squares and zones. The stressor decreased (P < 0.01) the time spent in close proximity (close zone; CZ) to conspecifics regardless of the familiarity of the stimulus birds. Regardless of treatment, test chicks showed shorter latencies to enter (P < 0.05) and spent longer time (P < 0.02) in the familiar than in the unfamiliar CZ suggesting that young chicks can discriminate between familiar and unfamiliar conspecifics encountered in novel surroundings. While in close proximity to familiar conspecifics, STR birds showed a reduced (P < 0.05) number of squares entered compared to CONs. This reduced locomotor activity was not accompanied by an increased activity in other zones of the runway. At the end of the trial, both CON and STR birds showed a reduced (P < 0.05) locomotor activity in the unfamiliar CZ and an increased (P < 0.05) activity in the central zone of the runway. Interestingly, no differences were detected between CON and STR birds in the total number of squares entered during the trial. These results suggest that prior stressor exposure did not affect the overall amount of locomotion but altered the spatial distribution of it. Collectively, our findings suggest that exposure to an acute stressor event subsequently affects chicks’ affiliation responses in runway tests. The way a bird will react depends on the identity (familiar or unfamiliar) of the conspecifics in its close environment.     

Fear responses in domestic chicks as a function of the social environment

The open field or novel environment has been used to assess fear in many species but its validity for the domestic fowl has recently been questioned. Based primarily on experiments which involved manipulation of the social environment Gallup and Suarez proposed that, contrary to an emotionality or fear interpretation, “open–field behaviour in chickens represents a compromise between opposing tendencies to reinstate contact with conspecifics and to minimize detection in the face of possible predation”. Predictions which can be made from the Gallup and Suarez model and from the fear hypothesis were tested by examining the effects of manipulating the social environment, during rearing and testing, on the open–field, hole–in–the–wall box and tonic immobility responses of domestic chicks. The results were inconsistent with predictions made from the Gallup and Suarez model but they conformed to the fear hypothesis. Furthermore, they were consistent with the majority of findings reported in the literature. Thus, while the opposing tendencies of reinstatement and predator evasion are, almost undoubtedly, important in many situations there remains considerable evidence for the role of fear in regulating the responses of domestic chicks to novel environments such as the open field. The two interpretations should not be considered mutually incompatible.     

Effects of social influence on neonatal approach responses of Gallus chicks

Although most laboratory studies of imprinting rear and test subjects individually, in the natural setting birds are imprinted in groups. In order to approximate and evaluate naturally occuring conditions, the present study compared the approach responses of chicks reared and trained alone to those reared and trained in pairs to an audio-visual imprinting stimulus. The responses of both groups were virtually identical during the presence of the imprinting stimulus. However, under conditions of experimental extinction, the paired trained birds (now tested alone) were more resistant to extinction than their isolated counterparts, thus suggesting that birds with prior social experience are more strongly imprinted than has been previously reported.     

The effects of the visual environment on responses to colour by domestic chicks

It is well known that development of vision is affected by experience, but there are few studies of environmental effects on colour vision. Natural scenes contain predominantly a restricted range of reflectance spectra, so such effects might be important, perhaps biasing visual mechanisms towards common colours. We investigated how the visual environment affects colour preferences of domestic chicks ( Gallus gallus), by training week-old birds to select small food containers distinguished from an achromatic alternative either by an orange or by a greenish-blue colour. Chicks that had been raised in control conditions, with long-wavelength-dominated reflectance spectra, responded more readily to orange than to blue. This was not due to avoidance of blue, as increasing saturation enhanced the chicks' preference for the same hue. The advantage of orange was, however, reduced or abolished for chicks raised in an environment dominated by blue objects. This indicates that responses to coloured food are affected by experience of non-food objects. If colours of ordinary objects in the environment do influence responses to specialised visual signals this might help explain why biological signals directed at birds are often coloured yellow, orange or red; long-wavelength-dominated spectra being more prevalent than short-wavelength-dominated spectra.     

The effects of regular handling on fear responses in the domestic chick

Reduction of fear in the domestic chick by regular handling was assessed and an attempt was made to determine whether such an effect was due specifically to reduced fear of human beings or to a general reduction in fearfulness. Regular handling decreased the tonic immobility response, a fear-potentiated phenomenon, and increased approach to a human being, but had no effect on approach towards an inanimate object. These findings were common to three strains (two layer, one broiler), and suggest that handling does not depress general fearfulness, but specifically reduces fear of human beings, presumably through habituation.     

Pubertal maturation and time of day differentially affect behavioral and neuroendocrine responses following an acute stressor

Puberty markedly influences stress responsiveness such that prepubertal animals show a more protracted corticosterone (CORT) and progesterone response following acute stress compared to adults. In both adult and juvenile rats, circadian time modulates adrenocortical steroids with basal CORT and progesterone levels rising prior to the onset of the dark phase of the light-dark cycle (i.e., active period). How time of day affects the pubertal difference in stress responsiveness and if the behaviors of prepubertal and adult animals are differentially affected by stress and time of testing remain unknown. Thus, we exposed group housed (3 per cage) prepubertal (28d) and adult (77d) male rats to 30 min of restraint in either the early portion of the behaviorally inactive, light (circadian nadir of CORT and progesterone) or behaviorally active, dark (circadian peak) phase of their light-dark cycle and measured ACTH, CORT, progesterone, and home cage behavior before and after the stressor. We found that the extended hormonal stress response demonstrated by prepubertal males occurred at both times of day. However, differences in post-stress behavior were dependent on time of testing. Specifically, although pre- and post-stress behaviors were similarly affected by the stressor in the light phase in prepubertal and adult males, during the dark phase, stress suppressed play behavior in the prepubertal males, and increased their time spent resting together (huddling), while these behaviors were unaffected by stress in the adults. These data indicate that pubertal development and time of day interact to modulate post-stress behavior and demonstrate a dissociation between post-stress hormonal and behavioral responses.     

Learning to fear and cope with a natural stressor: individually and socially acquired corticosterone and avoidance responses to biting flies

Animals learn to recognize and respond to a variety of dangerous factors, with biting and blood-feeding flies being among the most prevalent of natural stressors. Here we describe the behavioral avoidance and hormonal (corticosterone) stress responses to biting fly exposure and the roles of individual and social learning in the acquisition of these fear-associated responses. Male mice exposed to a single 30-min session of attack by intact biting flies (stable fly, Stomoxys calcitrans L.) exhibited increased plasma corticosterone levels and active self-burying responses to avoid the flies. When exposed 24 h later to altered flies whose biting mouth parts were removed and were incapable of biting, the mice displayed conditioned increases in corticosterone and avoidance responses. This conditioned increase in corticosterone and self-burying was also acquired through social learning without direct individual experience with the intact biting flies. Fly naive "observer" mice that witnessed other "demonstrator" mice being attacked by biting flies, but were not exposed to intact flies themselves, displayed increases in corticosterone levels and self-burying to avoid flies when exposed 24 h later to altered flies. The social learning was not due to social facilitation or sensitization. Observers had to witness the self-burying avoidance responses of the demonstrator to the biting flies in order to subsequently recognize a potential threat to themselves and display the appropriate responses. These individually and socially acquired conditioned fear responses are likely part of the mechanisms that allow animals to defend themselves from biting and blood-feeding arthropods.     

Open-field responses of domestic chicks in the presence or absence of familiar cues

Male domestic chicks were reared in groups with distinctive cues (red crosses) placed on the walls of the home boxes from 2 to 7 d of age and their subsequent behaviour in an open field in the presence or absence of the familiar rearing cues was recorded.Ambulation, peeping, pecking, jumping and standing were all significantly higher and the latency to the first step, duration of freezing, sitting time, lying time and time spent with the eyes closed were significantly lower when the familiar rearing cues were present in the test situation. These observations are consistent with the suggestion that the birds are less fearful in the presence of familiar stimuli. The presence of the familiar cues also increased the time spent feeding and drinking. The preference effect was a specific one, for birds exposed to red crosses in early life preferred such stimuli to black circles in a subsequent two-choice situation, whereas chicks reared with black circles preferred them to red crosses. There was no generalisation of attachment from one stimulus to the other. As the chicks spent more time feeding and drinking in the presence of the familiar cues, it is assumed that fear was reduced. Thus, the results tend to confirm that the frequency of certain behaviour patterns is indicative of certain levels of fear.     

Affiliation and social discrimination produced by brief exposure in day-old domestic chicks.

Discrimination between individual strangers and companions was examined in day-old domestic chicks. In one experiment, pecking rates at companions and strangers were observed in pairwise bouts after 16 hr of cohabitation. The discriminability of strangers and companions was varied by means of pre-hatch colouring. Reliable discriminations between individual strangers and companions emerged as early as the first minute of the encounter. Discriminative cues provided by artificial colouring were found not to be necessary in establishing social discrimination. In a second experiment, undyed chicks were housed in pairs for 1, 4 or 16 hr. Half of the pairs lived in cages that separated companions by a wire screen, and half were housed in undivided cages. Observations of pecking in four-way bouts confirmed previous findings and demonstrated that the opportunity to peck during exposure may be a necessary condition in producing social discrimination. Antecedent conditions that lead to the development of affiliative bonds simultaneously appear to establish social discrimination.     

Effects of duration of separation on responses to mates and strangers in the monogamous titi monkey (Callicebus moloch)

Adult male and female titi monkeys form an intense social bond characterized by high levels of affiliative interactions between pairmates and agonistic responses to strangers. In natural settings, separation between mates can vary from brief periods, as when mates drift apart during feeding, to permanent separation, occasioned by desertion or death. In this study we asked how different durations of separation altered the behavior of male and female titi monkeys (Callicebus moloch). We compared the effects of brief separation such as might occur incidentally during feeding (1–2 h) with prolonged separation such as might occur if one partner died or deserted (5 days). Effects were observed during a 30 min reunion of pairmates or during a 30 min encounter with a stranger of the opposite sex. Following brief separation, interactions between mates and between strangers clearly differed in measures of affiliation, but not in behaviors indicative of arousal. Following prolonged separation, measures of arousal increased with both mated pairs and strangers. Females tended to interact more readily with a stranger following prolonged separation than after brief separation, but interactions between mates were essentially unchanged and differed substantially from those between strangers. The data suggest that the pair bond persists in titi monkeys after prolonged social isolation, despite increased interest in interacting with potential new partners. Am. J. Primatol. 43:225–237, 1997. © 1997 Wiley-Liss, Inc.     

Tonic immobility and open field responses in domestic fowl chicks during the first week of life

The ontogeny of the tonic immobility (TI) response in domestic fowl chicks was studied during the first week of life. The TI response of naive White-Leghorn Gallus domesticus male chicks (N=5–9), was tested at the age of 1, 2, 3, 5 and 7 days. TI was induced dorsally and its duration, the number of induction trials and the latency of peeping were recorded. The TI response was strongly affected by age. It was poorly developed during the first 3 days of life, when the median TI duration in control chicks was 10 s and the mean number of induction trials 2.3±0.3. After the third day of life, TI duration increased by up to 15× and susceptibility by about two. Peeping latencies were very short throughout the first week and in many cases, peeping started long before the termination of TI. Immediately following recovery from TI, chicks were put in an open field and the latencies of walking and jumping and the number of steps, jumps and peeps were observed. No changes in either locomotion or vocalization in an open field were found between the third and fifth day. Furthermore, there was no correlation between any of the parameters of the TI and OF tests. The effect of habituation, which is known to attenuate the TI response, was studied by repeatedly subjecting chicks to TI and OF tests, once on each day of the experiment. Habituation prevented the increase in TI duration and susceptibility after the third day of life, but did not affect the OF response. The effect of aversive treatment, which was expected to increase TI, was examined by placing chicks in 5-cm deep tap water for 5 min, prior to testing. Treatment significantly attenuated TI on Day 1 and increased overall locomotion and peeping in open field.     

Impact of acute and chronic stressor experiences on heart atrial and brain natriuretic peptides in response to a subsequent stressor

The impact of stressful events on processes related to cardiovascular functioning might vary with previous stressor experiences, just as such sensitization effects have been detected with respect to several neurochemical and hormonal processes. The present investigation assessed the impact of a psychosocial stressor on factors directly or indirectly related to cardiovascular functioning among CD-1 mice that had previously experienced an acute or chronic stressor regimen. These factors included plasma variations of atrial and brain natriuretic peptides (ANP and BNP, respectively), inflammatory cytokines in plasma, mRNA expression of natriuretic peptides and inflammatory cytokines in the ventricles, and norepinephrine (NA) levels and utilization within the locus coeruleus, a brain region implicated in cardiac functioning. A social stressor (exposure to a dominant mouse) increased NE levels and utilization within the locus coeruleus, plasma corticosterone, cytokine and ANP levels. Among mice initially exposed to an acute stressor (restraint), NE utilization, ventricular ANP mRNA expression, and plasma interleukin-6 (IL-6) concentrations were markedly increased by the subsequent social stressor. In chronically stressed mice some of the effects of the social stressor were dampened, including changes of plasma corticosterone, locus coeruleus NE utilization, as well as plasma and ventricular IL-6 mRNA expression. Conversely, plasma ANP was markedly enhanced by the combined stressor events as was ventricular BNP and IL-1β mRNA expression. It seems that stressors may profoundly influence (sensitize or desensitize) on factors that could influence cardiovascular functioning. It remains to be determined whether these actions would be translated as pathophysiological outcomes.     

Animal models of social avoidance and social fear

Social fear and avoidance of social situations represent the main behavioral symptoms of social anxiety disorder (SAD), a highly prevalent anxiety disorder that is poorly elucidated and has rather unsatisfactory therapeutic options. Therefore, animal models are needed to study the underlying etiology and pathophysiology of SAD and to verify the efficacy of possible novel treatment approaches. In this review, we describe and discuss the most important paradigms that have been shown to induce social avoidance and fear in rodents, including foot shock exposure, restraint stress, social isolation, social instability, social defeat, conditioned defeat, social defeat/overcrowding, chronic subordinate colony housing, chronic mild stress, maternal separation and social fear conditioning. We also describe some of the behavioral paradigms used to assess social avoidance and fear in rodents, including the social interaction test, the social preference-avoidance test, the social approach-avoidance test, the three-chambered social approach test, the partition test and the modified Y-maze test. We focus on the behavioral alterations these paradigms induce, especially on social interaction, general anxiety and depressive-like behavior given that SAD is strongly comorbid with anxiety and affective disorders.     

Infants prefer the faces of strangers or mothers to morphed faces: an uncanny valley between social novelty and familiarity

The ‘uncanny valley’ response is a phenomenon involving the elicitation of a negative feeling and subsequent avoidant behaviour in human adults and infants as a result of viewing very realistic human-like robots or computer avatars. It is hypothesized that this uncanny feeling occurs because the realistic synthetic characters elicit the concept of ‘human’ but fail to satisfy it. Such violations of our normal expectations regarding social signals generate a feeling of unease. This conflict-induced uncanny valley between mutually exclusive categories (human and synthetic agent) raises a new question: could an uncanny feeling be elicited by other mutually exclusive categories, such as familiarity and novelty? Given that infants prefer both familiarity and novelty in social objects, we address this question as well as the associated developmental profile. Using the morphing technique and a preferential-looking paradigm, we demonstrated uncanny valley responses of infants to faces of mothers (i.e. familiarity) and strangers (i.e. novelty). Furthermore, this effect strengthened with the infant''s age. We excluded the possibility that infants detect and avoid traces of morphing. This conclusion follows from our finding that the infants equally preferred strangers’ faces and the morphed faces of two strangers. These results indicate that an uncanny valley between familiarity and novelty may accentuate the categorical perception of familiar and novel objects.     

Physiological and behavioral responses to strangers compared to friends as a source of disgust

Known as the source effect, feelings of disgust have been found to differ depending on the source of the disgusting material, with that emanating from oneself and familiar others eliciting less disgust than that of strangers. We tested the source effect on self-report of disgust feelings (Study 1), physiological response in heart rate (Study 2), and behavioral response in terms of approach–avoidance movement (Study 3). The results showed significantly higher levels of disgust feelings, more reduced heart rates, and faster avoidance behavior when processing disgusting material associated with strangers compared to that of familiar persons. Together these findings support the evolutionary view that disgust, as part of the human behavioral immune system to drive avoidance from disease-carrying agents, will likely be activated more intensely and quickly in response to unfamiliar as compared to familiar conspecifics who carry common germs more defendable by our shared physical immunity.     

From patterns to processes and back: analysing density-dependent responses to an abiotic stressor by statistical and mechanistic modelling

Our knowledge about population-level effects of abiotic stressors is limited, largely due to lack of appropriate time-series data. To analyse interactions between an abiotic stressor and density-dependent processes, we used experimental time-series data for stage-structured populations (the blowfly Lucilia sericata) exposed to the toxicant cadmium through 20 generations. Resource limitation results in competition both in the larval and the adult stages. The toxicant has only negative effects at the organism level, but nevertheless, there were positive population-level effects. These are necessarily indirect, and indicate overcompensatory density-dependent responses. A non-parametric model (generalized additive model) was used to investigate the density-dependent structures of the demographic rates, without making assumptions about the functional forms. The estimated structures were used to develop a parametric model, with which we analysed effects of the toxicant on density-dependent and density-independent components of the stage-specific demographic rates. The parameter estimates identified both synergistic and antagonistic density-toxicant interactions. It is noteworthy that the synergistic interaction occurred together with a net positive effect of the toxicant. Hence, the effects of such interactions should be considered together with the capacity for compensatory responses. The combination of the two modelling approaches provided new insight into mechanisms for compensatory responses to abiotic stressors.     

Differential responses of territorial Tawny Owls Strix aluco to the hooting of neighbours and strangers

Male Tawny Owls Strix aluco have individually distinct hooting calls. A classic play-back experimental design was used to examine the differences in behavioural responses of a known owl to the hooting of a neighbour (familiar) compared with a stranger (unfamiliar) in order to test the hypothesis that such hooting variations are used in calibrating interactions between conspecifics. We tested 12 male Tawny Owls and their mates; the overall intensity of agonistic response was significantly higher when we stimulated birds using playbacks of strangers than when we did so with those of neighbours. The behaviour displayed and the type of voice used by Tawny Owls were stronger toward strange males. Moreover, on the occasions we broadcast a strange male hooting, the singing rate was higher while the latency was lower.