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.     

Domestic chicks' runway responses to video images of conspecifics

Because chickens are highly social animals, live conspecifics are often used to provide an incentive or goal in studies of gait, sociality or fear that require the bird to traverse a runway. However, the variable behaviour of the stimulus birds can influence the approach/avoidance responses of the test birds and thereby confound the results. Because chickens modify their behaviour readily and appropriately to a variety of video images, including social stimuli, we asked if video playback might represent easily controllable and standardized alternatives to live birds. Female ISA Brown chicks were housed in groups of eight and then exposed to a blank illuminated television for 10 min per day from 2 to 7 days of age. At 8 or 9 days of age they were placed individually in the start box of a 1.6 m long runway and we recorded their responses to a monitor displaying selected video images that was situated in the goal box at the opposite end of the runway. In Experiment 1 chicks approached a monitor playing the video image and soundtrack of feeding chicks significantly sooner than one of a goal box with the food dish and background noise. In Experiment 2, chicks were exposed to the same video of feeding conspecifics with or without the associated sounds or to a video of the goal box with or without the chick soundtrack. Both the videos of other chicks elicited faster approach than did those of the goal box and the sound and silent versions were equally attractive. Adding the soundtrack of feeding chicks to the goal-box video failed to increase its attractiveness. The present results suggest that chicks are attracted towards televised images of other chicks. They also indicate that the visual and auditory components of the video stimuli did not exert additive effects and that approach reflected attraction to the visual image. Collectively, our findings suggest that video playback of selected social stimuli, such as feeding conspecifics, could be a valuable tool in tests requiring voluntary locomotion along a predetermined path.     

Selection of social traits in juvenile Japanese quail affects adults’ behaviour

The inability of animals to cope with their social environment in husbandry systems could be a major source of problems for both animal welfare management and economy. In this context, previous studies selected lines of domestic Japanese quail diverging for their level of social reinstatement, hypothesizing that quail with high levels of social motivation would adapt better to crowded social situations than quail with low levels of social motivation. However, these selections were based only on social motivation evaluated in young birds. As behavioural traits can vary with age, this study analysed the persistence of selected social traits into adulthood. With this in mind, we used several behavioural tests to estimate social motivation of adult females from selected lines for high social reinstatement (HSR, n = 24) and for low social reinstatement (LSR, n = 24). The tests were: open-field tests, emergence tests, separation tests, runway tests and confrontation tests. As birds’ behaviour in these tests can be influenced by the emotive characteristics of the subjects, we measured the emotional reactivity of quail not only during these tests but also in specific emotive tests: tonic immobility tests. Our results showed that the social motivation characteristics of birds persist in adulthood. Adult HSR females still presented a higher social motivation than adult LRS females: their response to social isolation was stronger and their motivation to reach conspecifics and to stay close to them was higher. However, the behavioural expression of social motivation appeared to be modified during development. Whereas vocal behaviour reflected the social motivation of chicks, in isolated contexts, this characteristic was not observed in adult quail.     

Fear and distress in Japanese quail chicks of two lines genetically selected for low or high adrenocortical response to immobilization stress.

Behavioral and adrenocortical reactivity to stressful stimulation was examined in 12- and 13-day-old chicks of two lines of Japanese quail selected over several generations for exaggerated (HS: high stress) or reduced (LS: low stress) plasma corticosterone (B) response to brief immobilization stress. Plasma B concentrations and tonic immobility (TI) fear reactions were measured in unstressed (control) and stressed (overnight cooping) chicks of both lines. The stress treatment was applied over a period of 12-20 hr and it involved capture by the experimenter, inescapable exposure to an unfamiliar environment and to strange conspecifics, reductions in ambient temperature and floor space, and the deprivation of food and water. Chicks of the HS line were more susceptible to the induction of TI and they remained immobile longer than did LS chicks. Therefore HS chicks were considered to be more fearful than their LS counterparts. Stress treatment elicited a marked adrenocortical response that was more pronounced in HS than in LS chicks. Stress treatment also increased susceptibility to TI but did not significantly affect the duration of immobility. These findings suggest that selecting the quail for differential corticosterone response to a particular stressor had exerted an unconscious and concomitant effect on underlying fearfulness as well as on their adrenocortical reactivity to several other stressful situations. The results are further discussed in terms of a putative relationship between adrenocortical activation and fearfulness.     

Ease of capture in lines of Japanese quail (Coturnix japonica) subjected to contrasting selection for fear or sociability

Japanese quail (Coturnix japonica) of lines, which have been subjected to contrasting selection for duration of the tonic immobility (TI) reaction or social reinstatement (SR) behaviour over many generations show corresponding differences in underlying fearfulness and sociality. As fearfulness and sociality are particularly influential traits in domesticated species, the finding that such traits respond to artificial selection may have important implications for poultry welfare and performance. However, it is not known if or how such selection has influenced human-animal interactions. The present experiment investigated the influence of fearfulness and SR behaviour on the ease with which birds could be caught and handled. Birds of lines selected for duration of the TI response or SR behaviour were reared in mixed line groups (LTI and STI or HSR and LSR) of 491 and 346 birds, respectively, until 6 weeks of age. When the birds were 2, 4, and 6 weeks of age, they were caught one by one and their individual capture ranks noted. In the group of birds selected for duration of the TI response, birds selected of the line selected for short duration of TI were caught before those selected for long duration of the response. In the group of birds selected for SR motivation, birds of the high line were caught before their low lines counterparts. Coefficients of concordance between capture ranks were significant and capture ranks did not differ significantly across ages. These results imply that selection for low levels of fear or high levels of sociality produces animals that are less disturbed by human interventions than animals selected for the opposite traits. The greater ease of capture of low fear line birds than high fear line birds may be explained by reduced fear of humans. The fact that the birds selected for high levels of SR behaviour are easier to catch than birds selected for low levels of sociality is less readily explicable. One hypothesis is that HSR line chicks tend to be more strongly imprinted on each other and the human caretaker. However, SR behaviour is highly species specific in both lines, existing evidence for line differences in social discrimination is limited and birds of the two lines show similar duration of the TI response. Despite this, whatever their underlying causation, these results demonstrate that genetic selection can be used to reduce negative reactions to human beings and may be of value in the improvement of both animal welfare and productivity.     

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.     

Social recognition and approach in the chick: lateralization and effect of visual experience

Chicks, Gallus gallus domesticus, tested monocularly on day 3 after hatching recognize familiar versus unfamiliar conspecifics and choose to approach one or other when they use the left eye, whereas they approach familiar and unfamiliar chicks at random when they use the right eye. In experiment 1 we investigated the effects of light exposure of embryos prior to hatching on this particular form of lateralization. Irrespective of whether they hatched from eggs incubated in the dark or from eggs exposed to light during the final days of incubation, chicks using the left eye had higher choice scores (meaning they chose to approach either a familiar or an unfamiliar chick) than chicks using the right eye or both eyes. Therefore, light experience prior to hatching did not influence the lateralization of individual recognition or choice behaviour, although it did affect latency to move out of, and time spent in, the centre of the runway. Experiment 2 showed that visual/social experience posthatching influences choice behaviour: chicks housed in a group in the light for 12 h on day 1 posthatching made a clear choice between familiar and unfamiliar chicks when tested on day 3, but chicks kept in a group in the dark on day 1 did not make a choice, instead alternating between the two stimuli. In experiment 3 we found that posthatching visual/social experience increased the choice scores of chicks using the right eye and thereby removed any lateralization of choice behaviour. The results suggest that visual experience of a social group is required before chicks using their right eye (and left hemisphere) will pay attention to the cues that distinguish one chick from another. Chicks using their left eye (and right hemisphere) recognize the difference between individuals without requiring visual experience with other chicks. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Trans-Generational Influence of Human Disturbances in Japanese Quail: Egg Quality Influences Male Social and Sexual Behaviour

In many bird species prenatal exposure to yolk androgens of maternal origin has been found to influence offspring behavioural phenotype. In contrast to altricial birds, far less is known about maternal effects in precocial birds. In a previous experiment we found that female quail ( Coturnix japonica ) that were not previously habituated to humans (NH) produced eggs with less androgens (testosterone, androstenedione) and more progesterone when exposed to human disturbances than females habituated to humans (H). Here, we analysed social motivation and sexual behaviour of the male offspring of NH and H females. Classical behavioural test procedures were applied including separation, runway, partner choice and female encounter tests. As chicks, offspring of the NH females spent more time far from conspecifics than offspring of the H females. As adults, the same NH males showed less crowing and courtship behaviour (ritual preening) in female encounter tests than H males. Thus, maternal environment and egg quality may be key factors in the emergence of individual variability of appetitive behaviour, such as social proximity and courtship behaviour. Human disturbance of the mother seems to have triggered trans-generational effects resulting in consistently reduced social and sexual motivation in offspring until adulthood.     

Domestication‐related variation in social preferences in chickens is affected by genotype on a growth QTL

A growth‐related QTL on chicken chromosome 1 has previously been shown to influence domestication behaviour in chickens. In this study, we used Red Junglefowl (RJF) and White Leghorn (WL) as well as the intercross between them to investigate whether stress affects the way birds allocate their time between familiar and unfamiliar conspecifics in a social preference test (‘social support seeking’), and how this is related to genotype at specific loci within the growth QTL. Red Junglefowl males spent more time with unfamiliar chickens before the stressful event compared to the other birds, whereas all birds except WL males tended to spend less time with unfamiliar ones after stress. A significant QTL locus was found to influence both social preference under undisturbed circumstances and social support seeking. The WL allele at this QTL was associated not only with a preference for unfamiliar individuals but also with a shift towards familiar ones in response to stress (social support seeking). A second, suggestive QTL also affected social support seeking, but in the opposite direction; the WL allele was associated with increased time spent with unfamiliar individuals. The region contains several possible candidate genes, and gene expression analysis of a number of them showed differential expression between RJF and WL of AVPR2 (receptor for vasotocin), and possibly AVPR1a (another vasotocin receptor) and NRCAM (involved in neural development) in the lower frontal lobes of the brains of RJF and WL animals. These three genes continue to be interesting candidates for the observed behavioural effects .     

Estimation of fear in two lines of the domestic chick: Correlations between various methods

The assessment of fear is a controversial issue and low levels of correlation between different measures have been used to criticise the fear concept. The present study assessed fear levels in individual domestic chicks of each of two lines, flighty and docile, using four commonly employed methods of estimating fear. They were the hole-in-the-wall box, the open field, response to a bell and tonic immobility. On the basis of a wide variety of behavioural responses each chick was ranked for fearfulness in each of the four tests. The degrees of association or correlation between these ranking within lines were then calculated. The significant intra-individual correlations found in both lines provides some support for the use of these tests as methods of estimating fear, at least within the lines used. Differences in the degree or form of fear-responding between the lines are also discussed in terms of reactions to handling and to sudden auditory stimuli.     

The relationship between social behaviour and habitat familiarity in African elephants (Loxodonta africana)

Social associations with conspecifics can expedite animals'' acclimation to novel environments. However, the benefits gained from sociality may change as the habitat becomes familiar. Furthermore, the particular individuals with whom animals associate upon arrival at a new place, familiar conspecifics or knowledgeable unfamiliar residents, may influence the type of information they acquire about their new home. To examine animals'' social dynamics in novel habitats, we studied the social behaviour of African elephants (Loxodonta africana) translocated into a novel environment. We found that the translocated elephants'' association with conspecifics decreased over time supporting our hypothesis that sociality provides added benefits in novel environments. In addition, we found a positive correlation between body condition and social association, suggesting that elephants gain direct benefits from sociality. Furthermore, the translocated elephants associated significantly less than expected with the local residents and more than expected with familiar, but not necessarily genetically related, translocated elephants. The social segregation between the translocated and resident elephants declined over time, suggesting that elephants can integrate into an existing social setting. Knowledge of the relationship between sociality and habitat familiarity is highly important in our constantly changing world to both conservation practice and our understanding of animals'' behaviour in novel environments.     

Selection for tonic immobility duration does not affect the response to novelty in quail

Genetic selection on a single fear test, the tonic immobility test, seems to result in selection on fearfulness, i.e. the propensity to exhibit fear responses, whatever the fear tests used. However, the conception of fear as a single variable has been challenged by the recognition that fear is multidimensional. This study was designed to test whether genetic selection on a classic index of fear in birds, tonic immobility duration, is accompanied by changes in the response to a single dimension of fear – novelty.Two lines of quail divergently selected for long (LTI) or short (STI) duration of tonic immobility were exposed to a novel object in their home cage. Quail of both lines showed typical fear reactions in response to novelty but there was no difference between lines. We conclude that genetic selection for tonic immobility duration does not affect all dimensions of fear, notably not novelty. Further studies are needed to investigate the dimensions of fear on which the two lines of quail could have been selected.     

Social learning in nest-building birds: a role for familiarity

It is becoming apparent that birds learn from their own experiences of nest building. What is not clear is whether birds can learn from watching conspecifics build. As social learning allows an animal to gain information without engaging in costly trial-and-error learning, first-time builders should exploit the successful habits of experienced builders. We presented first-time nest-building male zebra finches with either a familiar or an unfamiliar conspecific male building with material of a colour the observer did not like. When given the opportunity to build, males that had watched a familiar male build switched their material preference to that used by the familiar male. Males that observed unfamiliar birds did not. Thus, first-time nest builders use social information and copy the nest material choices when demonstrators are familiar but not when they are strangers. The relationships between individuals therefore influence how nest-building expertise is socially transmitted in zebra finches.     

Alarm responses are maintained during captive rearing in chicks of endangered kaki

The maintenance of species-specific behavioural repertoires and traditions is an important but often implicit goal of conservation efforts. When captive rearing is used as a conservation practice, it becomes critical to address its possible implications for the social and behavioural traits of developing individuals. In particular, animals must retain or acquire many of their behavioural abilities to increase the likelihood of survival upon release into the wild. This study investigated the behavioural development of critically endangered kaki (black stilt: Himantopus novaezelandiae ) chicks reared without live adult conspecifics. The captive rearing programme included playbacks of adult kaki alarm calls during cleaning and handling of precocial chicks housed as groups. We used videotaped observations and playback experiments to address the following questions: do kaki chicks respond differentially to (1) familiar versus unfamiliar adult kaki alarm calls and (2) conspecific alarm versus heterospecific control vocalizations. Adult-naïve kaki chicks exhibited a varied behavioural repertoire over their early development. In multivariate analyses, when age was statistically controlled, chicks showed responses to familiar and unfamiliar alarm calls that were similar in magnitude. In contrast, following conspecific alarm calls chicks had longer average latencies to resume pre-playback activities than following heterospecific vocalizations. Although the generality of these conclusions is limited by experimental constraints stemming from working with an endangered species, the findings suggest that current management techniques produce captive-reared kaki for release into the wild that possess many of the behavioural and auditory recognition skills that are required for survival.     

Enhanced yolk testosterone influences behavioral phenotype independent of sex in Japanese quail chicks Coturnix japonica

Studies have demonstrated an effect of yolk testosterone levels on the physiology and behavior of nestling birds. In order to investigate this phenomenon experimentally in a precocial bird, we enhanced yolk testosterone, but within the physiological range, by injecting 50 ng testosterone in ethanol into Japanese quail Coturnix japonica eggs prior to incubation. The chicks hatching from these as well as from control eggs that had received the carrier-only or were left unmanipulated were subject to a number of behavioral tests from hatching to the age of 3 weeks. In addition, fecal samples were taken during a 90-min isolation period to determine a physiological response to a stressor. Experimental chicks performed a detour task faster and approached novel objects sooner than did the controls. Chicks from treated eggs took a longer time to start distress vocalizing and also produced less distress calls during open-field trials, took on average a larger number of trials for them to show tonic immobility and also excreted lower levels of corticosterone metabolites (BM) than did the controls. In response to a stressor, excreted BM was initially higher in the control chicks, as compared to the experimental birds. Induced behavioral effects were independent of sex with no sex treatment interactions found. In sum, experimentally enhanced testosterone levels in the eggs shifted individual behavioral phenotype towards "bold" or "proactive", irrespective of sex. We conclude that testosterone in the yolk influences the coping style of hatchlings and may be a potential means of maternal influence on offspring phenotype.     

Experience with adults shapes multisensory representation of social familiarity in the brain of a songbird

Social animals learn to perceive their social environment, and their social skills and preferences are thought to emerge from greater exposure to and hence familiarity with some social signals rather than others. Familiarity appears to be tightly linked to multisensory integration. The ability to differentiate and categorize familiar and unfamiliar individuals and to build a multisensory representation of known individuals emerges from successive social interactions, in particular with adult, experienced models. In different species, adults have been shown to shape the social behavior of young by promoting selective attention to multisensory cues. The question of what representation of known conspecifics adult-deprived animals may build therefore arises. Here we show that starlings raised with no experience with adults fail to develop a multisensory representation of familiar and unfamiliar starlings. Electrophysiological recordings of neuronal activity throughout the primary auditory area of these birds, while they were exposed to audio-only or audiovisual familiar and unfamiliar cues, showed that visual stimuli did, as in wild-caught starlings, modulate auditory responses but that, unlike what was observed in wild-caught birds, this modulation was not influenced by familiarity. Thus, adult-deprived starlings seem to fail to discriminate between familiar and unfamiliar individuals. This suggests that adults may shape multisensory representation of known individuals in the brain, possibly by focusing the young's attention on relevant, multisensory cues. Multisensory stimulation by experienced, adult models may thus be ubiquitously important for the development of social skills (and of the neural properties underlying such skills) in a variety of species.     

Long-term effects of adolescent stress on neophobic behaviors in zebra finches are modulated by social context when in adulthood

Experiencing stress during adolescence can increase neophobic behaviors in adulthood, but most tests have been conducted in the absence of conspecifics. Conspecifics can modulate responses to stressors, for example by acting as ‘social buffers’ to attenuate the aversive appraisal of stressors. Here, we investigate the long-term effects of adolescent stress on the behavioral responses to novel stimuli (a mild stressor) across social contexts in an affiliative passerine bird, the zebra finch. During early (days 40–60) or late (days 65–85) adolescence the birds (n = 66) were dosed with either saline or the hormone corticosterone (CORT). CORT was given in order to mimic a physiological stress response and saline was given as a control. In adulthood, the birds' behavioral responses to a novel environment were recorded in both the presence and absence of conspecifics. An acute CORT response was also quantified in adolescence and adulthood. Our findings show clear evidence of social context mediating any long-term effects of adolescent stress. In the presence of familiar conspecifics no treatment effects were detected. Individually, birds dosed with CORT in early adolescence were slower to enter a novel environment, spent more time perching in the same novel environment, and, if female, engaged in more risk assessment. Birds dosed in late adolescence were unaffected. No treatment effects were detected on CORT, but adolescents had a higher CORT concentration than adults. Our results are the first to suggest that familiar conspecifics in adulthood can buffer the long-term effects of stress that occurred during early adolescence.     

Conspecific vocalisations,tonic immobility and fearfulness in the domestic fowl

Vocalisation is important in the transmission of fear/alarm among chickens. In this experiment, therefore, the effects of various conspecific calls on tonic immobility, a fear-potentiated, anti-predator response, were examined in adult laying hens. The shortest durations of immobility were observed after exposure to recordings of either the familiar background noise of the poultry house of ‘Ku’ calls which are normally associated with feeding. These stimuli exerted similar effects and both are considered more likely to attenuate rather than heighten fearfulness. Intermediate levels of immobility followed presentation of the post-laying cackle whereas recordings of warning calls, such as the aerial predator call, the ground predator call or the fear squawk, all significantly prolonged tonic immobility. The biological significance of these results is discussed in terms of fear and predator-defence.     

Genetic and phenotypic correlation between fluctuating asymmetry and two measurements of fear and stress in chickens

The purpose of the present study was to estimate the genetic and phenotypic correlation between fluctuating asymmetry and two measurements of fear and stress in chickens which had not deliberately stressed in any way, using the restricted maximum likelihood procedure. A total of 1073 36-week-old birds from two generations with complete pedigree of the Quail Castellana breed was used. Fluctuating asymmetry of several traits (leg, wing, and feather lengths, and ear-lobe and wattle areas), tonic immobility duration (indicator of fear), and heterophil to lymphocyte ratio (indicator of stress) were measured. The estimated genetic relationship between relative fluctuating asymmetry for the different traits and tonic immobility tended to be positive, that between the combined relative asymmetry of all traits and tonic immobility being near to +1; no significant phenotypic relationship was found between relative fluctuating asymmetry and tonic immobility. The genetic relationship between relative fluctuating asymmetry and heterophil to lymphocyte ratio was not consistent across the traits, ranging from +1 to −1, although the genetic correlation between the combined relative asymmetry and the heterophil to lymphocyte ratio was near to +1 too; no significant phenotypic relationship was found between relative fluctuating asymmetry and heterophil to lymphocyte ratio either. Relative fluctuating asymmetry and body weight were genetically negatively correlated for leg length and ear-lobe area but positively for feather length; the genetic correlation between the combined relative asymmetry and the body weight being near to −1; phenotypic relationships were not significantly different from zero. A significant negative genetic correlation between tonic immobility and heterophil to lymphocyte ratio was found, although the phenotypic association between these two measurements was zero. Phenotypic correlations always near to zero suggest that fluctuating asymmetry was not associated with duration of tonic immobility and heterophil to lymphocyte ratio in birds that have not been deliberately stressed.