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.

Trans-generational effects of prenatal stress in quail.

The prenatal environment is a source of phenotypic variability influencing the animal's characteristics. Prenatal stress affects not only the development of offspring, but also that of the following generation. Such effects have been best documented in mammals but can also be observed in birds, suggesting common processes across phylogenetic orders. We found previously that Japanese quail females stressed during laying produced offspring with higher fearfulness, probably related to modulation of testosterone levels in their eggs. Here, we evaluated long-term effects of prenatal stress by analysing reproductive traits of these F(1) offspring and, then, the development of their subsequent (F(2)) offspring. The sexual behaviour of F(1) prenatally stressed (F1PS) males was impaired. F1PS females' eggs contained less yolk and more albumen, and higher yolk testosterone and progesterone levels than did F(1) prenatal control females. The fearfulness of F(2) prenatally stressed quail was greater than that of F(2) prenatal control quail. These F(2) behavioural differences paralleled those evidenced by their parents, suggesting trans-generational transmission of prenatal stress effects, probably mediated by egg compositions of F1PS females.

On the significance of adult play: what does social play tell us about adult horse welfare?

Play remains a mystery and adult play even more so. More typical of young stages in healthy individuals, it occurs rarely at adult stages but then more often in captive/domestic animals, which can imply spatial, social and/or feeding deprivations or restrictions that are challenging to welfare, than in animals living in natural conditions. Here, we tested the hypothesis that adult play may reflect altered welfare states and chronic stress in horses, in which, as in several species, play rarely occurs at adult stages in natural conditions. We observed the behaviour (in particular, social play) of riding school horses during occasional outings in a paddock and measured several stress indicators when these horses were in their individual home boxes. Our results revealed that (1) the number of horses and rates of adult play appeared very high compared to field report data and (2) most stress indicators measured differed between 'players' and 'non-players', revealing that most 'playful' animals were suffering from more chronic stress than 'non-playful' horses. Frequency of play behaviour correlated with a score of chronic stress. This first discovery of a relationship between adult play and altered welfare opens new lines of research that certainly deserves comparative studies in a variety of species.

Differential outcomes of unilateral interferences at birth.

Behavioural modifications, including modifications of emotional reactivity, can occur following early experience such as handling (manual rubbing). Here, we investigated the effects of unilateral tactile stimulation at an early stage on emotional reactions later on. We handled newborn foals intensively on one side of their body. This early unilateral tactile experience had medium-term effects: the reactions of foals to a human approach, when they were 10 days old, differed according to the side stimulated at birth. Fewer right-handled foals accepted contact with humans, they delayed first contact longer and they evaded approaching humans sooner than did non-handled and left-handled foals. These results raise questions concerning the organization of neonatal care in animals and humans.

Reinforcement as a mediator of the perception of humans by horses (Equus caballus).

A central question in the interspecific human/animal relationship is how domestic animals perceive humans as a significant element of their environment. In this study, we tested the hypothesis that the use of positive or negative reinforcement in horse training may have consequences on the animals' perception of humans, as a positive, negative or neutral element. Two groups of ponies were trained to walk backwards in response to a vocal order using either positive or negative reinforcement. Heart rate monitors and behavioural observations were used to assess the animals' perception of humans on the short (just after training) and long (5 months later) terms. The results showed that the type of reinforcement had a major effect on the subsequent animals' perception of familiar and unfamiliar humans. Negative reinforcement was rapidly associated with an increased emotional state, as revealed by heart rate measurements and behavioural observations (head movements and ears laid back position). Its use led the ponies to seek less contact with humans. On the contrary, ponies trained with positive reinforcement showed an increased interest in humans and sought contact after training. This is especially remarkable as it was reached in a maximum of 5 sessions of 1 to 3 min (i.e. 5 to 15 min) and had lasting effects (visible after 5 months). Even learning was positively influenced by positive reinforcement. Overall, horses seem capable of associating humans to particular experiences and display extended long-term memory abilities.

Increased yolk testosterone facilitates prenatal perceptual learning in Northern bobwhite quail (Colinus virginianus).

Prenatal learning plays an important role in the ontogeny of behavior and birds provide a useful model to explore whether and how prenatal exposure to hormones of maternal origin can influence prenatal learning and the development of behavior. In this study we assessed if prenatal exposure to yolk testosterone can influence auditory learning in embryos of Northern bobwhite quail (Colinus virginianus). We experimentally enhanced testosterone concentrations in bobwhite quail eggs prior to incubation. The embryos from these T-treated eggs as well as control embryos that had received the vehicle-only or were non-treated were exposed to an individual bobwhite hen's maternal call for 120 min over the course of the day prior to hatching. All chicks were tested at 24 h following hatching for their auditory preference between the familiar bobwhite maternal call versus an unfamiliar bobwhite maternal call. T-treated chicks spent significantly more time in proximity to the familiar call compared to the unfamiliar call and also showed shorter latencies to approach the familiar call than control birds. Increased emotional reactivity, i.e. propensity to express fear responses, was also found in T-treated chicks. Baseline heart rates recorded in a second group of T-treated embryos and control embryos did not differ, which suggests no effect of yolk testosterone on baseline arousal level. To our knowledge this is the first demonstration of the influence of prenatal exposure to testosterone on auditory learning.

Adult: young ratio influences song acquisition in female European starlings (Sturnus vulgaris).

One parallel between humans and most songbirds is the fact that young require social interactions with an adult to acquire specific vocalizations. Songbirds are considered good models for comparative studies, although reports to date concern almost exclusively male songbirds. In addition, adult influence on vocal communication is generally investigated only in restricted social contexts (usually dyads). Here, the authors analyzed song learning and spatial associations among young female starlings that were maintained for 1 year in dyads (1 adult, 1 young), triads (2 adults, 1 young) or a larger group (7 young, 2 adults). Segregation by age was seen in the triads and in the larger group. The influence of adults (proportion of songs copied from adults) decreased as the young adult ratio increased. Unusual temporal features were observed in young maintained in triads and young neglected copying adult songs in the presence of peers. These results are among the first to explore the circumstances under which females learn and from whom they learn. They also add new insight to a wide range of questions about social influences on learning.

Habituation to humans affects yolk steroid levels and offspring phenotype in quail.

In the field as well as in the laboratory, human-generated stress responses are reduced in adult animals previously habituated to humans in comparison to non-habituated individuals. In birds, yolk steroid levels vary with maternal environment and condition. We tested the hypothesis that the experience of female birds with humans could affect yolk steroids levels and offspring phenotype. Two groups of Japanese quail, one habituated to humans (H) and a second non-habituated (NH), were exposed daily to brief human disturbances. We analysed egg quality, offspring growth, and offspring emotional reactivity. NH females produced eggs with less androgens (testosterone and androstenedione) and more immunoreactive progesterone compared to birds habituated to humans. NH females produced eggs with less yolk, heavier shell and chicks hatching later and being smaller as compared to habituated individuals. A lower emotional reactivity was found in young of NH females compared to young of H females. Thus, human disturbance of the mother triggered different effects on chick phenotype depending on previous experience of mother birds with humans. In addition, we describe for the first time the influence of environmental stimuli on yolk immunoreactive progesterone levels. Our results show that a relatively minor difference in behavioral habituation may have substantial effects on eggs and offspring. This has obvious implications for keeping and handling laboratory animals, for conservation biology and for animal welfare.

Laterality and emotions: visual laterality in the domestic horse (Equus caballus) differs with objects' emotional value.

Lateralization of emotions has received great attention in the last decades, both in humans and animals, but little interest has been given to side bias in perceptual processing. Here, we investigated the influence of the emotional valence of stimuli on visual and olfactory explorations by horses, a large mammalian species with two large monocular visual fields and almost complete decussation of optic fibres. We confronted 38 Arab mares to three objects with either a positive, negative or neutral emotional valence (novel object). The results revealed a gradient of exploration of the 3 objects according to their emotional value and a clear asymmetry in visual exploration. When exploring the novel object, mares used preferentially their right eyes, while they showed a slight tendency to use their left eyes for the negative object. No asymmetry was evidenced for the object with the positive valence. A trend for an asymmetry in olfactory investigation was also observed. Our data confirm the role of the left hemisphere in assessing novelty in horses like in many vertebrate species and the possible role of the right hemisphere in processing negative emotional responses. Our findings also suggest the importance of both hemispheres in the processing positive emotions. This study is, to our knowledge, the first to demonstrate clearly that the emotional valence of a stimulus induces a specific visual lateralization pattern.

Could adults be used to improve social skills of young horses, Equus caballus?

We investigated the effects of the introduction of foreign adults on the behavior of young horses. First, we observed the behavior of 1- and 2-year-old domestic horses housed in same-age and same-sex groups (a standard housing system, but different from a natural situation). Then, two same-sex adults were introduced into each experimental group. Observations made before, during and after an introduction indicated that young horses reared in homogeneous groups of young had different behaviors compared to other domestic horses reared under more socially natural conditions. After the introduction of adults, young horses expressed new behaviors, preferential social associations emerged, positive social behavior increased and agonistic interactions decreased. These results have important implications both for understanding the influence that adults may have on the behavior of young horses, and in terms of husbandry, indicating the importance of keeping young horses with adults, although further studies are still necessary.

First suckling: a crucial event for mother-young attachment? an experimental study in horses (Equus caballus).

This study investigates the consequences of interference during first suckling for subsequent mare-young attachment in horses (Equus caballus). Foals brought to their dams' teats appeared, at later ages (1-3 months), to remain closer to their dams and to play less than control foals that had been allowed to suckle spontaneously. Higher levels of play and distance initiatives from the mother are considered criteria for secure attachment in horses, humans, and other species. As this unique handling was the only event that distinguished experimental from control groups, the authors concluded that first suckling is a crucial event in the development of secure dam-young attachment. These results could have important implications for all mammal species, including humans.

Stable individual profiles of daily timing of migratory restlessness in European quail.

Temporal characteristics of migratory behavior in birds are usually studied at the species and population levels, and rarely at the individual level. Variations among species and populations of the seasonal onset of migratory behavior have been widely investigated, but very little is known about its daily organization or whether birds are conservative in their behavior. The determination of intra- and inter-individual variability is important for the study of genetic variations and can reveal the existence of different adaptation capacities within populations. This laboratory study analyzed intra- and inter-individual variability of daily initiation and time course of nocturnal restlessness in partial-migrant European quail (Coturnix coturnix coturnix). Thirty-five quail were selected randomly from a captive stock, and their spring activity was recorded under natural daylenghs. Eighteen of the thirty-five quail presented behavioral profiles of migrant birds. Migrant birds initiated their nocturnal activity punctually, and the time courses of the nocturnal activity of 88% of them revealed intra-individual stability over six consecutive nights. All birds initiated their nocturnal activity after sunset and civil twilight, and they were more active at the beginning than the middle or end of the night, suggesting that their drive to migrate could be synchronized with particular skylight conditions. For the first time, stable individual profiles in the daily time course of migratory restlessness are shown. These results support previous findings concerning biological rhythms of quail and raise questions concerning the timing of migratory behavior.

Maternal food calling in domestic hens: influence of feeding context.

The aim of this study was to understand the relationship between production of food calls by maternal hens and food context. In a series of experiments with broody hens, we manipulated quality of items, quantity of food, food experience and dispersion of food items. We measured the frequency of food calling during standardized tests. Our results show that all the variables tested had significant effects on food calling. These results present some similarities and some discrepancies with previous reports on food calling by cockerels.

Mothering influences the distribution of activity in young domestic chicks.

The aim of this study was to determine whether the presence of a maternal hen influences the quality, quantity, and distribution of activity in young chicks. Brooded and nonbrooded chicks were observed during the entire light phase when they were 4 d of age. Our results revealed that although both brooded and nonbrooded chicks expressed the same behavioral items and in quite the same quantity, activity bouts were much longer in brooded chicks. However, only brooded chicks presented a high level of ultradian rhythmicity. Moreover, the brooded chicks made greater use of the space. The presence and the behavior of maternal hens appeared to provide structuring factors for the expression of the chicks behavior.

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.

Age affects the expression of maternal care and subsequent behavioural development of offspring in a precocial bird.

Variations of breeding success with age have been studied largely in iteroparous species and particularly in birds: survival of offspring increases with parental age until senescence. Nevertheless, these results are from observations of free-living individuals and therefore, it remains impossible to determine whether these variations result from parental investment or efficiency or both, and whether these variations occur during the prenatal or the postnatal stage or during both. Our study aimed first, to determine whether age had an impact on the expression of maternal breeding care by comparing inexperienced female birds of two different ages, and second, to define how these potential differences impact chicks' growth and behavioural development. We made 22 2-month-old and 22 8-month-old female Japanese quail foster 1-day-old chicks. We observed their maternal behaviour until the chicks were 11 days old and then tested these chicks after separation from their mothers. Several behavioural tests estimated their fearfulness and their sociality. We observed first that a longer induction was required for young females to express maternal behaviour. Subsequently as many young females as elder females expressed maternal behaviour, but young females warmed chicks less, expressed less covering postures and rejected their chicks more. Chicks brooded by elder females presented higher growth rates and more fearfulness and sociality. Our results reveal that maternal investment increased with age independently of maternal experience, suggesting modification of hormone levels implied in maternal behaviour. Isolated effects of maternal experience should now be assessed in females of the same age. In addition, our results show, for first time in birds, that variations in maternal care directly induce important differences in the behavioural development of chicks. Finally, our results confirm that Japanese quail remains a great laboratory model of avian maternal behaviour and that the way we sample maternal behaviour is highly productive.

Yolk testosterone levels and offspring phenotype correlate with parental age in a precocial bird.

Parents, and particularly mothers, can influence their offspring's development in non-genetic ways. Maternal effects can occur during the mothering phase as well as during the embryonic phase. Prenatal maternal effects in birds can be mediated by yolk steroid hormones that influence subsequent offspring development. Studies have focused mainly on the influence of laying females' living conditions on yolk hormonal contents, and rarely on the effects of individual characteristics. Here, we investigated prenatal influence of parent age on yolk steroid levels and on offspring phenotype. We compared Japanese quail at two different ages: at the beginning of their reproductive cycle (11 weeks old: age 1) and six months later, after egg production peak (37 weeks old: age 2). Egg composition, reproductive outcomes, and offspring growth, sexual development and behaviour were studied at both ages. We found that laying rate, fertility and chick survival rates declined between age 1 and age 2. Age 2 eggs had relatively lighter shells and higher yolk plus albumen contents; they also had lower testosterone contents. Age 2 offspring weighed more at hatching than did age 1 offspring; subsequently their growth patterns differed and their sexual development was more precocious. Age 2 offspring were less emotional than age 1 offspring when encountering a novel environment, and they appeared more sensitive to social separation. Our study shows, for the first time in a bird species, a strong impact of parental age on offspring phenotype, and especially on behaviour, an impact that is possibly mediated via modulation of yolk testosterone content.

Adults may be used to alleviate weaning stress in domestic foals (Equus caballus).

The present study aims to investigate whether the presence of unrelated adult horses at weaning would reduce the social stress of weaning and the emergence of undesirable behaviours. We tested this hypothesis in 32 domestic foals by comparing short and medium term behavioural and physiological responses to weaning in foals maintained in homogeneous groups of peers (PW) to those of foals grouped with both peers and unrelated adults (AW). In total, three trials were conducted, which each trial consisting of one AW group and one PW group. In all foals, weaning was followed by increased vocalization, increased locomotion and increased salivary cortisol concentration. However, signs of stress were less pronounced and shorter in duration in weanlings housed with unrelated adults (e.g., whinnies: p<0.05; salivary cortisol: p<0.05). Only foals without adults exhibited increased aggressiveness towards peers (p<0.05) and abnormal behaviours (p<0.05) such as excessive wood-chewing and redirected sucking towards peers. In conclusion, introducing adults to minimize weaning stress in foals and later on aggressiveness and abnormal behaviours appears as the most promising approach to date.

Japanese quail's genetic background modulates effects of chronic stress on emotional reactivity but not spatial learning.

Chronic stress is known to enhance mammals' emotional reactivity and alters several of their cognitive functions, especially spatial learning. Few studies have investigated such effects in birds. We investigated the impact of a two-week stress on Japanese quail's emotional reactivity and spatial learning. Quail is an avian model widely used in laboratory studies and for extrapolation of data to other poultry species. As sensitivity to chronic stress can be modulated by intrinsic factors, we tested juvenile female Japanese quail from three lines, two of them divergently selected on tonic immobility duration, an indicator of general fearfulness. The different emotional reactivity levels of quail belonging to these lines can be revealed by a large variety of tests. Half of the birds were submitted to repeated unpredictable aversive events for two weeks, whereas the other half were left undisturbed. After this procedure, two tests (open field and emergence tests) evaluated the emotional reactivity of treated and control quails. They were then trained in a T-maze for seven days and their spatial learning was tested. The chronic stress protocol had an impact on resting, preening and foraging in the home cage. As predicted, the emotional reactivity of treated quails, especially those selected for long tonic immobility duration, was higher. Our spatial learning data showed that the treatment enhanced acquisition but not memorization. However, intrinsic fearfulness did not seem to interact with the treatment in this test. According to an inverted U-shaped relationship between stress and cognition, chronic stress can improve the adaptability of birds to a stressful environment. We discussed the mechanisms possibly implied in the increase of emotional reactivity and spatial abilities.

Do horses have a concept of person?

BACKGROUND: Animals' ability for cross-modal recognition has recently received much interest. Captive or domestic animals seem able to perceive cues of human attention and appear to have a multisensory perception of humans. METHODOLOGY/PRINCIPAL FINDINGS: Here, we used a task where horses have to remain immobile under a vocal order to test whether they are sensitive to the attentional state of the experimenter, but also whether they behave and respond differently to the familiar order when tested by a familiar or an unknown person. Horses' response varied according to the person's attentional state when the order was given by an unknown person: obedience levels were higher when the person giving the order was looking at the horse than when he was not attentive. More interesting is the finding that whatever the condition, horses monitored much more and for longer times the unknown person, as if they were surprised to hear the familiar order given by an unknown voice. CONCLUSION/SIGNIFICANCE: These results suggest that recognition of humans may lie in a global, integrated, multisensory representation of specific individuals, that includes visual and vocal identity, but also expectations on the individual's behaviour in a familiar situation.