Drink safely: common swifts (Apus apus) dissipate mechanical energy to decrease flight speed before touch-and-go drinking.

Flight is an efficient way of transport over a unit of distance, but it can be very costly over each unit of time, and reducing flight energy expenditure is a major selective pressure in birds. The common swift (Apus apus) is one of the most aerial bird species, performing most behaviours in flight: foraging, sleeping and also drinking by regularly descending to various waterbodies and skimming over the surface. An energy-saving way to perform such touch-and-go drinking would be to strive to conserve mechanical energy, by transforming potential energy to kinetic energy during the gliding descent, touching water at high speed, and regaining height with minimal muscular work. Using 3D optical tracking, we recorded 163 swift drinking trajectories, over three waterbodies near Rennes, France. Contrary to the energy conservation hypothesis, we show that swifts approaching a waterbody with a higher mechanical energy (higher height and/or speed 5 s before contact) do not reach the water at higher speeds, but do brake, i.e. dissipate mechanical energy to lose both height and speed. Braking seems to be linked with sharp turns and the use of headwind to some extent, but finer turns and postural adjustments, beyond the resolving power of our tracking data, could also be involved. We hypothesize that this surprisingly costly behaviour results from a trade-off between energy expenditure and safety, because approaching a water surface requires fine motor control, and high speed increases the risk of falling into the water, which would have serious energetic and survival costs for a swift.

Impact of natural and artificial prenatal stimulation on the behavioural profile of Japanese quail.

As the sensory systems of vertebrates develop prenatally, embryos perceive many environmental stimuli that can influence the ontogeny of their behaviour. Whether the nature and intensity of prenatal stimuli affect this ontogeny differently remains to be investigated. In this context, this study aimed to analyse the effects of prenatal auditory stimulation (natural stimulation, NS; predator vocalisations or artificial stimulation, AS; metallic sounds) on the subsequent behaviour of young Japanese quail (Coturnix coturnix japonica). For this, behavioural variables recorded during ethological tests evaluating emotional and social reactivity were analysed using a principal component analysis. This analysis revealed significant differences between the behavioural profile of stimulated chicks and that of non-exposed chicks. Indeed, chicks exposed to NS expressed more intense emotional responses in fearful situations, but less neophobia when exposed to a novel environment or object, whereas chicks exposed to AS appeared more sensitive to social isolation. Our results show that the acoustic environment of embryos can influence the way young birds subsequently interact with their social and physical environment after hatching, and face challenges in changing living conditions.

Prenatal maternal stress is associated with behavioural and epigenetic changes in Japanese quail.

Prenatal maternal stress (PMS) influences many facets of offspring's phenotype including morphology, behaviour and cognitive abilities. Recent research suggested that PMS also induced epigenetic modifications. In the present study, we analysed, in the Japanese quail, the effects of PMS on the emotional reactivity and cognitive abilities of the F1 offspring. We also investigated in the hippocampus, the paraventricular hypothalamic nucleus and subnuclei of the arcopallium/amygdala the level of two histone post-translational modifications, H3K4me2 and H3K27me3, known to be impacted by stress. We found that PMS does not affect F1 quail's learning abilities but increases their emotional reactivity. Moreover, we demonstrated that PMS induced an increased density of H3K27me3 positive cells, in the hippocampus, paraventricular hypothalamic nucleus and dorsal nucleus of the amygdala, but not variations of H3K4me2. As these brain regions are involved in the control of vertebrates' emotional responses, the effect of PMS on the epigenetic mark H3K27me3 could possibly be a mechanism involved in the behavioural effects we observed in F1 quail.

Fos expression in the medial preoptic area and nucleus accumbens of female Japanese quail (Coturnix japonica) after maternal induction and interaction with chicks.

The neural system underlying maternal caregiving has often been studied using laboratory rodents and a few other mammalian species. This research shows that the medial preoptic area (mPOA) integrates sensory cues from the young that, along with hormonal and other environmental signals, control maternal acceptance of neonates. The mPOA then activates the mesolimbic system to drive maternal motivation and caregiving activities. How components of this neural system respond to maternal experience and exposure to young in non-mammals has rarely been examined. To gain more insight into this question, virgin female Japanese quail (Coturnix japonica) were induced to be maternal through four days of continuous exposure to chicks (Maternal), or were not exposed to chicks (Non-Maternal). Chicks were removed overnight from the Maternal group and half the females from each group were then exposed to chicks for 90 minutes (Exposed), or not exposed to chicks (Non-Exposed), before euthanasia. The number of Fos-immunoreactive (Fos-ir) cells was examined as a marker of neuronal activation. As expected, repeated exposure to chicks induced caregiving behavior in the Maternal females, which persisted after the overnight separation, suggesting the formation of a maternal memory. In contrast, Non-Maternal females were aggressive and rejected the chicks when exposed to them. Exposed females, whether or not they were given prior experience with chicks (i.e., regardless if they accepted or rejected chicks during the exposure before euthanasia), had more Fos-ir cells in the mPOA compared to Non-Exposed females. In the nucleus accumbens (NAC), the number of Fos-ir cells was high in all Maternal females whether or not they were Exposed to chicks again before euthanasia. In the lateral bed nucleus of the stria terminalis, a site involved in general stress responding, groups did not differ in the number of Fos-ir cells. These data indicate a conserved role for the mPOA and NAC in maternal caregiving across vertebrates, with the mPOA acutely responding to the salience rather than valence of offspring cues, and the NAC showing longer-term changes in activity after a positive maternal experience even without a recent exposure to young.

Chicks from stressed females elicit overprotective behaviour in adoptive mother quail.

Beyond the genetic links between mother and young, prenatal effects experienced by offspring can modulate their mother's behaviour and stress. Here we investigated the consequences of stress-induced prenatal maternal effects on quail chicks' behaviour and maternal behaviour. We evaluated how adoptive quail mothers (unstressed) raised chicks of females that had either been stressed (PS) or were non-stressed (NPS) during laying. We demonstrated previously that our social stress procedure during laying increases levels of egg yolk steroid and chicks' emotional reactivity during the postnatal period. We found that, compared to NPS mothers, PS mothers remained closer to their chicks, were aggressed and neglected them less, emitted more maternal vocalisations and called their chicks more when they were separated. Moreover, PS chicks made more requests on their mother. Our results show that mothers responded to chicks' behavioural changes caused by prenatal stress by adapting their maternal behaviour. As exemplified here, for the first time in birds, prenatal environment can affect postnatal maternal behaviour by changing their offspring's behaviour.

The development of flight behaviours in birds.

Flight is a unique adaptation at the core of many behaviours in most bird species, whether it be foraging, migration or breeding. Birds have developed a wide diversity of flight modes (e.g. flapping, gliding, soaring, hovering) which involves very specialized behaviours. A key issue when studying flight behaviours is to understand how they develop through all the ontogenetic stages of birds, from the embryo to the flying adult. This question typically involves classical debates on animal behaviour about the importance of maturation and experience. Here, we review the literature available on the development of flight behaviours in birds. First, we focus on the early period when young birds are not yet capable of flight. We discuss examples and show how endogenous processes (e.g. wing flapping in the nest, flight development timing) and environmental factors (e.g. maternal stress, nutritional stress) can influence the development of flight behaviours. Then, we review several examples showing the different processes involved in the development of flight in flight-capable juveniles (e.g. practice, trial and error learning, social learning). Despite the lack of experimental studies investigating this specific question at different developmental stages, we show that several patterns can be identified, and we anticipate that the development of new tracking techniques will allow us to study this question more thoroughly in more bird species.

Mother-chick interactions are affected by chicks' sex and brood composition in Japanese quail.

Sex is a trait which leads mothers to invest asymmetrically in their young, especially in species with a strong dimorphism. Authors usually consider that members of the largest sex require the most investment by mothers. In other cases, mothers care preferentially for members of the sex that increase their fitness, e.g. males, in numerous species. In quail, a precocial bird, mother seems to take more care of their males which are more sensitive to their separation. This study investigates the influence of chicks' sex and brood's sexual composition on the maternal behavior of quail. We evaluated three batches of mothers, composed of (a) unisex broods of males (MM), (b) unisex broods of females (FF), and (c) mixed sex broods (Mx). We recorded mother-chick interactions during 11 days of mothering. We found that MM mothers spent more time warming their chicks and FF mothers were more active. Moreover, females rejected more aggressively and earlier their female chicks than their male chicks. Finally, Mx chicks, whatever their sex, interacted more with their mothers. Our results highlight a greater quantity and quality of maternal care towards male. Mothers invest more in male chicks. We discussed results in terms of each sex's needs.

High social motivation induces deficits in maternal behaviour but not plasticity of the subventricular zone in Japanese quail (Coturnix japonica).

Maternal behaviour develops differently depending on the characteristics of an individual, such as age or emotional reactivity. Social motivation, defined as the propensity to establish social contact, has received little attention in relation to maternal behaviour in birds. In addition, the transition to motherhood is a time of plasticity in the brain of the new mother in mammals. However, it remains to be determined how maternal brain plasticity is affected in avian species. The present study investigated how a the social motivation of a mother alters maternal behaviour and brain plasticity of the Japanese quail (Coturnix japonica). Adult females from lines selected for high and low social motivation were exposed to chicks for 11 days. After maternal care testing, and at matched time points in controls, the brains of females were perfused for assessment of doublecortin-immunoreactive staining, a marker of neurogenesis, in the subventricular zone (SVZ), a neurogenic niche. The results obtained showed that high socially motivated female quail spent significantly less time performing maternal behaviour when exposed to chicks compared to low socially motivated females. Moreover, the warming of chicks by high socially motivated females involved less covering postures and mothers were more rejecting of chicks. Interestingly, the plasticity indicators in the SVZ did not differ between low and high socially motivated females and were not associated with differences in maternal caregiving when using doublecortin-immunoreactive staining. Thus, high social motivation in this avian species does not favour maternal behaviour and this level of motivation to the mother is not related to changes in neuroplasticity in the SVZ of the female quail.

Human behaviour at the origin of maternal effects on offspring behaviour in laying hens (Gallus gallus domesticus).

Regular visual presence of humans is known to reduce chickens' human-generated stress responses. Here we questioned whether, more than mere visual presence, human behaviour affects laying hen behaviour and subsequently their offspring's behaviour. We hypothesized that human behaviour triggers maternal effects via variations in yolk hormone levels. For five consecutive weeks, two groups of hens were exposed to the same durations of human presence (30 min twice a day, five days a week) but the behaviour of the human differed between groups. The first group (H+) was exposed to predictable arrival of the experimenter, slow movements combined with static presence, stroking during handling and human voice. Whereas the second group of hens (H-) was exposed to unpredictable arrival of the experimenter which remained silent, in motion, and did not provide stroking during handling. At the end of the treatment, we evaluated egg quality and offspring behaviour. We found that avoidance of the experimenter by H+ hens but not by H- hens decreased significantly. Fertility rates and concentrations of yolk progesterone and estradiol in H+ hens' eggs were higher than in H- hens' eggs. Fear of humans, neophobia or the capacity to solve a detour task did not differ significantly between H+ and H- chicks. Social discrimination tests showed that H+ chicks but not H- chicks typically preferred a familiar conspecific to a stranger. These results show that, with the same duration in the presence of the birds, humans through their behaviour engender variations in fertility rates, yolk hormone levels and transgenerational effects on social skills. Rarely explored, our data suggest that maternal effects influence filial imprinting. These data have broad implications for laboratory, commercial systems and conservatory programs where the inevitable presence of humans could trigger maternal effects on offspring phenotype.

Incubation temperature affects the expression of young precocial birds' fear-related behaviours and neuroendocrine correlates.

The influence of embryonic microclimate on the behavioural development of birds remains unexplored. In this study, we experimentally tested whether chronic exposure to suboptimal temperatures engendered plasticity in the expression of fear-related behaviours and in the expression of the corticotropin-releasing factor in the brains of domestic chicks (Gallus g. domesticus). We compared the neurobehavioural phenotypes of a control group of chicks incubated in an optimal thermal environment (37.8 °C) with those of a group of experimental chicks exposed chronically in ovo to suboptimal temperatures (27.2 °C for 1 hour twice a day). Chronic exposure to a suboptimal temperature delayed hatching and decreased growth rate and experimental chicks had higher neophobic responses than controls in novel food and novel environment tests. In addition, experimental chicks showed higher expression of corticotropin-releasing factor than did controls in nuclei of the amygdala, a structure involved in the regulation of fear-related behaviours. In this study, we report the first evidence of the strong but underappreciated role of incubation microclimate on the development of birds' behaviour and its neurobiological correlates.

Maternal care affects chicks' development differently according to sex in quail.

Maternal behavior is known to influence the behavioral development of young. Recently, it was demonstrated that maternal behavior also differed according to sex of chicks and brood sex composition. So, here, we explored if these factors influenced behavioral development of quail chicks when they were brooded, and what characteristics of chicks and foster females could best explain this development. We studied three sets of chick pairs brooded by foster females: unisex male, unisex female, and mixed broods. We found that both emotivity profile and sociality depended on the sex: females were more reactive and less social than males. Females' emotivity profile was correlated with brood composition and foster female activity during maternal care. In males, only sociality was correlated with foster females' scores of aggressive rejection. Our results evidence that male and female chicks respond differentially to maternal behavior. This is discussed in terms of ecological and physiological constraints on development according to sex.

Lipids in maternal diet influence yolk hormone levels and post-hatch neophobia in the domestic chick.

We assessed whether the ratio of dietary n-6/n-3 polyunsaturated fatty acids (PUFA) during egg formation engenders transgenerational maternal effects in domestic chicks. We analyzed yolk lipid and hormone concentrations, and HPA-axis activity in hens fed a control diet (high n-6/n-3 ratio) or a diet enriched in n-3 PUFAs (low n-6/n-3 ratio) for 6 consecutive weeks. Their chicks were tested for neophobia during the first week of life. We found higher corticosterone metabolites in droppings of hens fed the diet enriched in n-3 and significantly higher concentrations of yolk progesterone, androstenedione, and estradiol in their eggs compared to controls. Chicks of hens fed the n-3 enriched diet showed a lower body mass at hatch than controls and expressed higher neophobia when exposed to a novel object. These results add support to the hypothesis that the nutritional state of female birds produces variation in yolk hormone levels and engender maternal effects.

Brood size can influence maternal behaviour and chick's development in precocial birds.

Mothers have a crucial influence on offspring development. Variations of maternal behaviour can be due to numerous parameters, for instance costs are related to the size of a brood/litter, which in turn can influence the level of mothers' investment in each offspring. Here we investigated the influence of brood size on the behaviour of Japanese quail mothers and chicks during the mothering period and on offspring development. We compared two types of broods: small broods of three chicks (N=9) and large broods of six chicks (N=9). Behavioural tests assessed chicks' social and emotional traits. Mothers of large broods emitted more maternal vocalisations at the beginning of the mothering period, but at the end they assumed more non-covering postures and trampled chicks more than mothers of small broods. Chicks in large broods huddled up more whereas chicks in small broods rested alone more frequently. Moreover, the social motivation of chicks in large broods was higher than that of chicks in small broods, although their emotional reactivity levels were similar. Our results evidence the importance of brood size for maintaining family cohesion and the influence of brood size on chicks' interactions with their siblings. We evaluated the influence of mothers and siblings on chicks' behavioural development.

3D tracking of animals in the field using rotational stereo videography.

We describe a method for tracking the path of animals in the field, based on stereo videography and aiming-angle measurements, combined in a single, rotational device. In open environments, this technique has the potential to extract multiple 3D positions per second, with a spatial uncertainty of <1 m (rms) within 300 m of the observer, and <0.1 m (rms) within 100 m of the observer, in all directions. The tracking device is transportable and operated by a single observer, and does not involve any animal tagging. As a video of the moving animal is recorded, track data can easily be completed with behavioural data. We present a prototype device based on accessible components that achieves about 70% of the theoretical maximal range. We show examples of bird ground and flight tracks, and discuss the strengths and limits of the method, compared with existing fine-scale (e.g. fixed-camera stereo videography) and large-scale tracking methods (e.g. GPS tracking).

Long-life partners or sex friends? Impact of parental pair bond on offspring personality.

Previous investigations reported that some traits of parental relationships, including pair-bond duration or mate behavioural compatibility, influence subsequent offspring fitness by acting on their behaviour and growth and thus their early survival. We hypothesized that the development of a pair bond between sexual partners would have a prenatal influence. This study investigated the impact of two pairing managements on the egg characteristics and development of offspring of Japanese quail (Coturnix c. japonica). Thirty males and 30 females were paired either continuously (C; mates together all the time) or non-continuously (NC; pairs met only three times a week for 5 min). Separation-reunion tests evaluated parental pair bond. Egg yolk testosterone and androstenedione levels were evaluated, and the somatic and behavioural development of C and NC chicks was assessed. Our results revealed that members of C pairs were attached to their mates and, although no significant differences in androgen levels could be evidenced between egg sets, a higher proportion of C pairs' eggs were fertilized and their chicks appeared less emotive and more social. Our results revealed that the parental relationship can modulate the behavioural development of their offspring, probably via non-genetic effects, and this could play a major role in the emergence of inter-individual variability.

Fearfulness affects quail maternal care and subsequent offspring development.

Our study investigated relationships between a precocial bird's fearfulness and maternal care, and the implication of maternal care as a vector for non-genomic transmission of fearfulness to chicks. We compared care given to chicks between two sets of female Japanese quail selected to present either high (LTI) or low fearfulness (STI). Chicks, from a broiler line, were adopted by these females following a sensitization procedure. Chicks' fearfulness after separation from their mother was assessed by well-established procedures. LTIs took longer to present maternal responses, pecked chicks more during the first days post-hatch, presented impaired maternal vocal behaviour and were globally less active than STI females. Chicks mothered by LTIs presented more fearful reactions than did chicks mothered by STIs, supporting the hypothesis of a non-genetic maternal transmission of fearfulness. We suggest that the longer latencies required by LTIs to become maternal are a consequence of their greater fear of chicks, and that their lower general and vocal activity could be components of a heightened antipredatory strategy. We discuss the transmission of maternal fearfulness to fostered chicks, taking into account the possible implication of several well-known mechanisms underlying maternal effects.

Precocial bird mothers shape sex differences in the behavior of their chicks.

Compared to mammals and altricial birds, evaluations of differences related to precocial birds' sex have often been limited to sexual behavior. Nevertheless, the extensive use of precocial bird models for investigating behavioral development issues requires in depth knowledge concerning the emergence of sex differences. Here, we evaluated behavioral differences between Japanese quail chicks in relation to their sex. We know that maternal influences are strong and early social environment shapes behavioral development in this species. Therefore, we investigated the emergence of sex differences in two very different early social situations to evaluate the impact of precocial bird mothers on sex differences. We assessed behavioral differences related to sex of (1) non-brooded chicks and of (2) brooded chicks, using various ethological tests to evaluate emotional reactivity and social motivation differences related to sex. Our results show that both non-brooded and brooded chicks present behavioral differences related to sex. They differed greatly according to chicks' early experience. Sex-related differences between maternally deprived (non-brooded) chicks concerned mainly fearfulness, whereas differences between male and female brooded chicks concerned mainly their reactions to social isolation. We hypothesize that mothers attenuate sex differences related to fearfulness by being a model for responses to fear-eliciting situations and by providing a similar secure basis to both males and females. We finally propose that mothers induce differences in chicks' sociality by providing asymmetrical care toward males and females.

Short- and long-term effects of unpredictable repeated negative stimuli on Japanese quail's fear of humans.

Numerous aversive events occur in poultry production, and if repeated and unpredictable, can result in an impaired welfare. Some events such as handling can be perceived negatively and it is of interest to understand how humans' behaviour could affect poultry's behaviours and especially its avoidance of humans. Our aim was to evaluate short- and long-lasting effects of a 3-week procedure involving unpredictable repeated negative stimuli (URNS) applied during the post-juvenile period on quail's reactivity to humans. We compared the reactions of two sets of quail: URNS was applied to one set (treated quail) and the other set was left undisturbed (control quail). When two weeks old, treated quail were exposed to a variety of negative stimuli, either applied automatically or involving human presence. One and seven weeks after the termination of the procedure, the reactivity of control and treated quail to a passive human being was evaluated. Furthermore, the experimenter with her hand on a trough containing a mealworm assessed the propensity of quail of both groups to habituate to feed close to a human being. In the presence of a seated observer, treated quail were more inhibited and more alert than control quail. Likewise, seven weeks after the end of the URNS procedure, more treated than control quail adopted a fear posture. Moreover, whereas control quail spent as much time in the different areas of their cages, treated quail spent more time in the rear part of their cages. Finally, whereas control quail habituated gradually to feed near the experimenter's hand, treated quail did not. All these tests evidence negative short- and long-term effects on treated quail's reactivity to a passive human being and on their habituation to a human being when her presence is positively reinforced. This highlights the importance of young poultry's experience with humans in production.

Emotionality modulates the effect of chronic stress on feeding behaviour in birds.

Chronic stress is a long-lasting negative emotional state that induces negative consequences on animals' psycho-physiological state. This study aimed at assessing whether unpredictable and repeated negative stimuli (URNS) influence feeding behaviour in quail. Sixty-four quail were exposed to URNS from day 17 to 40, while 64 quail were undisturbed. Two lines divergently selected on their inherent emotionality were used to assess the effect of genetic factors on the sensitivity to URNS. All quail were submitted to a sequential feeding procedure (using two diets of different energetic values) which placed them in a contrasting situation. Behavioural tests were performed to assess the emotional reactivity of the two lines. Results confirmed that differences exist between them and that their emotional reactivity was enhanced by URNS. Diet preferences, motivation and daily intake were also measured. URNS did not change the preferences for the hypercaloric diet compared to the hypocaloric diet in choice tests, but they reduced daily intakes in both lines. Motivations for each diet were differently affected by URNS: they decreased the motivation to eat the hypercaloric diet in quail selected for their low inherent fearfulness whereas they increased the motivation to eat the hypocaloric diet in quail selected for their high inherent fearfulness, which suggested a devaluation process in the former and a compensatory behaviour in the later. Growth was furthermore reduced and laying delayed by URNS in both lines. In conclusion, the exposure to URNS induced interesting changes in feeding behaviour added with an increase in emotional reactivity and an alteration of production parameters. This confirms that both lines of quail experienced a chronic stress state. However differences in feed motivation and emotional reactivity between lines under chronic stress suggested that they experienced different emotional state and use different ways to cope with it depending on their genetic background.

Motherless quail mothers display impaired maternal behavior and produce more fearful and less socially motivated offspring.

Early maternal deprivation impairs the behavioral development of young individuals. Recently, strong differences between mothered and maternally deprived chicks have been reported concerning their emotionality, sociality, and spatial skills. Here we investigated long-term and cross-generational impacts of maternal deprivation by comparing the characteristics of the non-reproductive and the maternal behavior of 22 mothered and 22 non-mothered adult female Japanese quail (Coturnix c. japonica) and by comparing the behavior of their respective fostered chicks. We reveal that non-brooded mothers were more fearful and less competent in spatial tasks and expressed impaired maternal care, characterized by more aggression towards chicks, higher activity rates, and more abnormal pacing during the first days of the care period. Chicks' behavior was clearly affected by maternal care inducing strong differences in their fearfulness and social motivation. Our results show both long-term and cross-generational impacts of early maternal deprivation in precocial birds.