Animal-to-robot social attachment: initial requisites in a gallinaceous bird.

Animal-Robot Interaction experiments have demonstrated their usefulness to understand the social behaviour of a growing number of animal species. In order to study the mechanisms of social influences (from parents and peers) on behavioural development, we design an experimental setup where young quail chicks, after hatching, continuously live with autonomous mobile robots in mixed triadic groups of two chicks and one robot. As precocial birds are subject to imprinting, we compare groups where chicks meet the robot as their very first social partner, on their first day after hatching (R chicks), with groups where chicks meet a real conspecific first (C chicks), and the robot later (on the second day after hatching). We measured the behavioural synchronization between chicks and robot over three days. Afterwards, we directly tested the existence of a possible social bond between animal and robot, by performing separation-reunion behavioural tests. R chicks were more synchronized with the robot in their daily feeding-resting activities than C chicks. Moreover, R chicks emitted numerous distress calls when separated from the robot, even in the presence of another chick, whereas C chicks emitted calls only when separated from the other chick. Whether the observed chick-robot attachment bond reflects filial, or sibling-imprinting of chicks towards the robot remains unclear, as the latter process is not fully understood in natural familial groups. Still, these results reveal the necessary initial conditions for stable, cohesive mixed groups of chicks and robots, a promising tool to experiment on the long-term dynamics of social behaviour.

Environmental enrichment reduces behavioural alterations induced by chronic stress in Japanese quail.

Animals perceiving repeated aversive events can become chronically stressed. Chronic activation of the hypothalamic-pituitary-adrenal (HPA) axis can have deleterious consequences on physiological parameters (e.g. BW, blood chemistry) and behaviour (e.g. emotional reactivity, stereotypies, cognition). Environmental enrichment (EE) can be a mean to reduce animal stress and to improve welfare. The aim of this study was first, to assess the effects of EE in battery cages on the behaviour of young Japanese quail and second, to evaluate the impact of EE on quail exposed to chronic stress. The experiment involved quail housed in EE cages and submitted or not to a chronic stress procedure (CSP) (EE cages, control quail: n=16, CSP quail: n=14) and quail housed in standard cages and exposed or not to the CSP (standard non-EE cages, control quail: n=12, CSP quail: n=16). Our procedure consisted of repeated aversive events (e.g. ventilators, delaying access to food, physical restraint, noise) presented two to five times per 24 h, randomly, for 15 days. During CSP, EE improved quail's welfare as their stereotypic pacing decreased and they rested more. CSP decreased exploration in all quail. After the end of CSP, quail presented increased emotional reactivity in emergence test. However, the effect of EE varied with test. Finally, chronic stress effects on comfort behaviours in the emergence test were alleviated by EE. These results indicate that EE can alleviate some aspects of behavioural alterations induced by CSP.

Effect of mothering on the spatial exploratory behavior of quail chicks.

Previous maternal deprivation experiments demonstrated that absence of maternal care impacts the behavioral development of young animals. Here we assessed the influence of the presence of a mothering hen on the spatial exploration of Japanese quail chicks, after the mothering period. Brooded and nonbrooded chicks were placed in a novel environment containing feeding troughs. The distribution of chicks and their inter-individual distances were measured during repeated tests. Brooded chicks exhibited a higher ability to disperse, thereby progressively exploiting larger surfaces and gaining access to food more easily. The fact that exploration by nonbrooded chicks was delayed suggests a deficit in their exploratory motivation and/or spatial skills. We hypothesize that brooded chicks experienced the constraint to follow the mothering hen, and to adapt to frequent reconfigurations of their environment. The lack of this variability in the environment of nonbrooded chicks could have reduced adaptability of their spatial behavior.

Influence of a mobile robot on the spatial behaviour of quail chicks.

Quail chicks encountered an autonomous mobile robot during their early development. The robot incorporated a heat source that stimulated following of chicks. The spatial behaviour of grown-up chicks was tested in an exploration test and a detour test. Chicks that grew with the mobile robot exhibited better spatial abilities than chicks grown with a static heat source. We discuss these results in the perspective of animal-robot interaction and of the role of early spatial experience on the behavioural development.

Higher inherent fearfulness potentiates the effects of chronic stress in the Japanese quail.

There is considerable variability in the susceptibility of individuals to the adverse effects of chronic stress. In humans and other mammals, individual traits such as high anxiety are proposed as a vulnerability factor for the development of stress-related disorders. In the present study, we tested whether a similar behavioural trait in birds, higher emotional reactivity, also favours the occurrence of chronic stress-related behavioural and physiological dysfunction. For this, lines of Japanese quail divergently selected for a typical fear response in birds, the duration of tonic immobility, were subjected to unpredictable aversive stimulation over 2 weeks. Previous studies demonstrate that the selection program modifies the general underlying emotionality of the birds rather than exerting its effect only on tonic immobility. Interestingly, only birds selected for their higher emotionality exhibited significantly enhanced latency to first step and decreased locomotor activity in the open-field test after exposure to chronic stress compared to non-stressed control birds. This effect of chronic stress was selective for the tested dimension of bird emotional reactivity because there was no observed effect on the tonic immobility response. Moreover, chronically stressed birds selected for their higher emotionality exhibited significantly decreased basal corticosterone levels, a physiological marker of stress. These findings show that chronic stress is associated with changes in emotional reactivity and related physiological markers in birds. They also highlight emotional reactivity as an important predisposing factor for the occurrence of the adverse effects of chronic stress in birds.

Effect of melatonin supplementation on the sexual development in European quail (Coturnix coturnix).

At the end of their wintering phase, male European quails were exposed to a stimulation photoperiod of light/dark 12:12 h for 10 days to induce sexual development. A daily oral melatonin supplementation was then given to one group of treated males (N=11) and the alcohol solvent was given to a control group of males (N=10). These solutions were provided during the final 3 h of the photophase for 28 days, then during the final 4 h for 18 days. There were no significant differences between the two groups with respect to fat levels. However, 3 weeks after the beginning of melatonin supplementation, the sexual development of the treated birds slowed down. The importance of this decline varied to a greater or lesser degree between individual birds. When melatonin supplementation stopped, sexual development resumed. Activity recordings revealed a decrease in feeding activity when melatonin supplementation was provided. However, this response showed important interindividual variability. The birds that produced the most marked responses to melatonin during the first 3 weeks of supplementation were those that also showed the most obvious decline in sexual development. It seems that, in European quail, a wild migratory species that always shows a natural biological annual rhythm, a melatonin signal could play a role in regulating reproduction.

Ontogeny of the ultradian rhythm of activity in Japanese quail.

As soon as they hatch, gallinaceous chicks follow broody hens. This matriarchal unit presents a temporal organization of activity. The ontogeny of this ultradian rhythm of activity was followed in Japanese quail during their first 3 weeks of life. Under controlled laboratory conditions, 12 groups of four chicks were recorded using an activity monitoring system. They were observed between the ages of 2 and 17 days. Chicks in groups presented an ultradian rhythm of activity, with a period that increased significantly from 14.3 +/- 1.4 minutes when chicks were 2 days old to 26.0 +/- 1.9 minutes when they were 16 days old. The increase of ultradian periodicity was particularly pronounced during their first and third weeks of life. Finally, the ultradian period was correlated positively with body weight of the chicks.

Circadian rhythm of activity during the annual phases in the European quail, Coturnix coturnix.

Migratory birds, such as the European quail, present an annual cycle with the following phases: moult, fattening, migration and reproduction. This study aimed at determining how variations in the circadian rhythm of feeding during the annual cycle took endogenous rhythmic characteristics into account. The birds (n = 8) were maintained under constant dim light from the age of 1 to 9 months. Feeding activity was recorded using infra-red detectors. The birds expressed all the phases, except migration. Activity was arrhythmic when they were moulting. A circadian rhythm of feeding activity appeared during the fattening phase. In males, the circadian period lengthened and the clarity of the rhythm increased during sexual development. These results appear to confirm the effects of physiological state on the temporal organisation of activity. Variations of the circadian rhythm could influence the ability to synchronize with exogenous cycles such as the alternation of day and night.

Induction of circadian rhythm of feeding activity by testosterone implantations in arrhythmic Japanese quail males.

Studies in vertebrates have shown that hormones can influence circadian rhythms of behavior. We investigated whether testosterone could induce rhythmicity in arrhythmic Japanese quail, kept in DD. The animals used were 3 1/2-week-old castrated males from a line of quail selected for the lack of the circadian rhythm of feeding activity. After 3 weeks in DD, 8 birds were implanted with an empty implant and 16 others with a testosterone implant. Two weeks later, the operation was repeated. After implantation, we noticed that 15 out of 16 testosterone-treated birds showed a circadian rhythm of feeding activity, in contrast to the control birds, which remained arrhythmic. The clarity of this rhythm increased significantly after each implantation. A positive correlation was found between the indexes of clarity of the rhythm (autocorrelation coefficient ratio and area of the peak of spectrum) and the plasma testosterone level. The period of the induced free-running rhythm was identical to the specific value of the endogenous circadian rhythm in immature quail. The circadian period showed a significant lengthening with the second implantation. This lengthening looks like the variation previously observed in maturing rhythmic or implanted quail. So, it would appear that testosterone can act on rhythmicity on at least two levels: by inducing the circadian rhythm and increasing its clarity and by modulating its period. To explain these results, several hypotheses can be considered. First, the observed arrhythmy may be the consequence of an internal desynchronization of oscillators, responsible for generating the circadian rhythm of feeding activity, and testosterone could play a role in the coupling of these oscillators. Alternatively, we suggest that testosterone could act on the transcription of genes implicated in the control of the rhythmicity or may regulate by rapid signals the cellular rhythmic activity. The possible functional values of the enhancing of circadian rhythmicity by testosterone at different stages of the bird's life were discussed.

Circadian rhythm of activity in Japanese quail in constant darkness: variability of clarity and possibility of selection.

In conditions of constant darkness, interindividual variability in the clarity of circadian rhythmicity was observed in sexually immature young quail, with birds classified as more or less rhythmic or arrhythmic. The relative clarity of this circadian rhythm was observed on the actograms by measurement of the autocorrelation coefficient ratio over 12 cycles. Autocorrelation coefficients were calculated from sequential series of total activity over 12-minute periods. Crosses of selected phenotypes with different clarities of rhythmicity were conducted in order to study the possibility of selection of this characteristic. From a random population (N = 42, twice), pairs of the most rhythmic birds (3 families), and pairs of arrhythmic birds (4 families) were reared. Autocorrelation coefficient ratios of F1 birds from rhythmic families (N = 54) were greater than those of F1 birds (N = 48) from arrhythmic families (t-test, p < .0001). These ratios in offspring were significantly correlated with that of the mean parent of each clutch of siblings (N = 102, r = .35, p = .0003). This result was maintained in a second generation (F2) of birds, for which significant differences in expressed rhythmicity were observed. That is, autocorrelation coefficient ratios of F2 birds from two rhythmic families (N = 30) were greater than those of F2 birds from arrhythmic families (N = 20) (t-test, p = .039). Comparison of F2 outbred and inbred birds from rhythmic pairs showed greater values of autocorrelation coefficient ratios in the case of inbred birds (N = 16) than for outbred birds (N = 30; t-test, p = .036). There was no difference between outbred (N = 20) and inbred birds (N = 15) from arrhythmic pairs. Therefore, selection of a rhythmic strain seems possible, whereas crosses between two arrhythmic birds may also give rise to rhythmic birds. Comparisons between rhythmic birds of different families did not show differences in the free-running period of the circadian rhythm, which is true also for rhythmic birds bred from two arrhythmic parents. Therefore, our selection procedure did not seem to be based on the characteristics of the pacemaker itself, but rather on a downstream event. Although the parents were not selected on the basis of quantity of activity per cycle or on the duration of the active phase, significant differences among the offspring of different families were shown.