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.     

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.     

Correlated response in yolk testosterone levels following divergent genetic selection for social behaviour in Japanese quail

Maternal effects are a powerful tool that parents can use to modify the phenotype of their offspring. In birds, the amount of androgens that females deposit in their eggs has been shown to influence early development and adult behavioural phenotypes. Differences in such behavioural strategies have been used as the target of artificial selection programmes with a view to improve animal welfare. In this study, we tested whether artificial selection for divergent social behaviour in Japanese quail had resulted in correlated changes in yolk androgen levels. We used lines that had been selected at the chick stage for high and low motivation to regain contact with a group of conspecific chicks. This procedure has led to important behavioural differences in the high and low line in a suite of behavioural correlates of sociality. We found that eggs laid by the line selected for high motivation for social reinstatement contained more than twice the amount of yolk testosterone of eggs laid by females from the low line, while the unselected line laid eggs with intermediate levels. This finding strongly suggests a functional link between these two traits, and underlines the possible role of yolk androgen modulation in promoting the evolution of behavioural syndromes.     

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.     

Maternal Epigenetic Transmission of Social Motivation in Birds

Behavioural development is a complex phenomenon involving interactions between genetic constraints and environmental influences. One of the most potent environmental influences during the ontogeny of the behavioural characteristics of young is played by mothers. In particular, mammalian mothers modulate the social competences of their young, influencing all their future social life. Here, we investigated the influence of the social characteristics of adoptive mother birds ( Coturnix coturnix japonica ) on the social motivation (origin of every social relationship) of the young they reared. We characterized the social behaviour of standard stock chicks reared by female quail, genetically selected either for low (LSR) or high (HSR) levels of social reinstatement (index of treadmill behaviour which combined the tendency to run towards conspecifics with the tendency to move away from them), to investigate epigenetic transmission of social motivation. Our results show that HSR and LSR adoptive mothers partially transmitted their social characteristics to their young: chicks reared by HSR females presented higher levels of social motivation than chicks reared by LSR females. This maternal influence appeared much clearer in young males than in young females. Our study reveals that, as in mammals, bird mothers influence epigenetically the development of the social behaviour of their young.     

Development of fearfulness in birds: genetic factors modulate non-genetic maternal influences

The development of fearfulness and the capacity of animals to cope with stressful events are particularly sensitive to early experience with mothers in a wide range of species. However, intrinsic characteristics of young animals can modulate maternal influence. This study evaluated the effect of intrinsic fearfulness on non-genetic maternal influence. Quail chicks, divergently selected for either higher (LTI) or lower fearfulness (STI) and from a control line (C), were cross-fostered by LTI or STI mothers. Behavioural tests estimated the chicks' emotional profiles after separation from the mother. Whatever their genotype, the fearfulness of chicks adopted by LTI mothers was higher than that of chicks adopted by STI mothers. However, genetic background affected the strength of maternal effects: the least emotional chicks (STI) were the least affected by early experience with mothers. We demonstrated that young animal's intrinsic fearfulness affects strongly their sensitivity to non-genetic maternal influences. A young animal's behavioural characteristics play a fundamental role in its own behavioural development processes.     

Effect of female brooding behaviour on male mate choice in Japanese quail, Coturnix japonica

Brooding behaviour is a likely cue to a female's reproductive status and therefore a potentially important factor in male mate assessment. We induced brooding behaviour in adult female Japanese quail by exposure to foster chicks for five 20-min trials over 3 days. In two experiments, we assessed the influence of this brooding behaviour on male mate choice in Japanese quail using an established mate choice paradigm. In each experiment we gave males a choice between two females presented simultaneously and measured preference by the time spent in proximity to each. In the first experiment, a male's preference for the initially preferred female significantly decreased after he had seen her brooding three chicks. In the control condition, male preference for an initially preferred female remained relatively consistent over consecutive trials if he did not see her brood chicks. These results suggest that females who are brooding chicks are less attractive to male Japanese quail. Further evidence from the second experiment substantiates this finding, and strongly suggests that males are averse to behavioural cues from maternal females, rather than the mere presence of chicks. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Mothering during early development influences subsequent emotional and social behaviour in Japanese quail

The aim of the present study was to investigate the influence of mothers on the emotional reactivity and social behaviour in young precocial Japanese quail. We used a classical method of maternal deprivation. Ethological tests and observations analysed and compared the behaviour of young artificially raised quail to that of young raised by adoptive maternal quail. After separation from mothers, brooded young were more fearful (frightened easily) in the presence of humans (human-observer tests) and more neophobic in novel environments (open-field and hole-in-the-wall tests) than young raised artificially. As chicks rarely expressed fear during the brooding period, no differences related to mothering could be observed at that time. In separation tests, brooded chicks jumped significantly more frequently than non-brooded chicks and later, observations of groups revealed that brooded chicks remained closer to one another than non-brooded chicks. Social motivation of brooded chicks appeared to be higher. These results indicate that, during their first days of life, mothers influence the emotional and social behaviour of their young.     

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.     

Immediate early gene expression associated with induction of brooding behavior in Japanese quail

Certain species can be induced to foster infant or neonatal animals through the process of sensitization. We induced brooding behavior in adult Japanese quail through repeated exposure to foster chicks across five 20-min trials. Brooding behavior was characterized by a bird allowing chicks to approach and remain underneath its wings while assuming a distinctive stationary crouching posture, preening, and feather fluffing. Birds who did not show brooding behavior actively avoided chicks. Among the birds that brooded chicks, females brooded chicks for longer durations compared to males. Brooding females continued a regular daily egg laying pattern; males showed no significant changes in testosterone levels after exposure to chicks. In a second experiment, we measured expression of two immediate early gene (IEG) protein products, ZENK and Fos, to identify the brain regions activated or inhibited by brooding behavior in females. ZENK and Fos expression in brooding or sensitized females (SF) were compared with expression in nonmaternal females with chicks (NMF) and with females without chicks and with blocks as control objects (BL). There was a reduced density of ZENK-like immunoreactive (ZENK-lir) cells in the medial preoptic nucleus (POM) in NMF birds. In SF birds, the density of Fos-like immunoreactive (Fos-lir) cells was elevated in the bed nucleus stria terminalis, medial portion (BSTm), and ectostriatum (E). These experiments begin to define the neural circuitry underlying brooding behavior in Japanese quail, and establish a model for future studies of the neural mechanisms of avian parental behavior.     

Social instability in laying quail: consequences on yolk steroids and offspring's phenotype

Individual phenotypic characteristics of many species are influenced by non-genetic maternal effects. Female birds can influence the development of their offspring before birth via the yolk steroid content of their eggs. We investigated this prenatal maternal effect by analysing the influence of laying females' social environment on their eggs' hormonal content and on their offspring's development. Social instability was applied to groups of laying Japanese quail females. We evaluated the impact of this procedure on laying females, on yolk steroid levels and on the general development of chicks. Agonistic interactions were more frequent between females kept in an unstable social environment (unstable females) than between females kept in a stable social environment (stable females). Testosterone concentrations were higher in unstable females' eggs than in those of stable females. Unstable females' chicks hatched later and developed more slowly during their first weeks of life than those of stable females. The emotional reactivity of unstable females' chicks was higher than that of stable females' chicks. In conclusion, our study showed that social instability applied to laying females affected, in a non-genetic way, their offspring's development, thus stressing the fact that females' living conditions during laying can have transgenerational effects.     

Heritability and genetic correlations of fear-related behaviour in Red Junglefowl--possible implications for early domestication

Domesticated species differ from their wild ancestors in a number of traits, generally referred to as the domesticated phenotype. Reduced fear of humans is assumed to have been an early prerequisite for the successful domestication of virtually all species. We hypothesized that fear of humans is linked to other domestication related traits. For three generations, we selected Red Junglefowl (ancestors of domestic chickens) solely on the reaction in a standardized Fear of Human-test. In this, the birds were exposed for a gradually approaching human, and their behaviour was continuously scored. This generated three groups of animals, high (H), low (L) and intermediate (I) fearful birds. The birds in each generation were additionally tested in a battery of behaviour tests, measuring aspects of fearfulness, exploration, and sociality. The results demonstrate that the variation in fear response of Red Junglefowl towards humans has a significant genetic component and is genetically correlated to behavioural responses in other contexts, of which some are associated with fearfulness and others with exploration. Hence, selection of Red Junglefowl on low fear for humans can be expected to lead to a correlated change of other behavioural traits over generations. It is therefore likely that domestication may have caused an initial suite of behavioural modifications, even without selection on anything besides tameness.     

Ultradian Rhythm of Activity in Japanese Quail Groups under Semi-Natural Conditions during Ontogeny: Functional Aspects and Relation to Circadian Rhythm

The function of ultradian rhythms is not yet clearly elucidated. In particular, short-term rhythms are expressed during early ontogeny, especially in broods of precocial birds. We investigated the relationship between the clarity of the ultradian rhythm of the activity/rest cycle of a group of young Japanese quail (Coturnix japonica) and the level of social synchronisation and spatial cohesion between the birds within that group. The subjects were descended from two lines selected for either very pronounced rhythmic or arrhythmic circadian activity. We found a positive relationship between the clarity of the ultradian rhythm of the activity/rest cycle when birds were young and the clarity of the circadian rhythm of feeding activity when birds were older, but still immature. The temporal organisation of the behaviour of the chicks from these two lines was observed in outdoor aviaries, when they were 4, 8, 12 and 15 days old. The mean ultradian period expressed by groups of 12 chicks was variable, with a minimum of 6 minutes. The ultradian period lengthened regularly as chicks grew older, and reached approximately 40 min on day 15. The clarity of the ultradian rhythmicity of group activity was linked to the level of inter-individual social synchronisation and of spatial cohesion; the more pronounced the ultradian rhythms of a group, the greater the temporal and spatial cohesion of the chicks within the group. Moreover, these characteristics varied with the age of the chicks. Finally, chicks in the less rhythmic groups weighed less. These results stress the adaptive value of this temporal organisation strategy under natural conditions.     

Ultradian Rhythm of Activity in Japanese Quail Groups under Semi-Natural Conditions during Ontogeny: Functional Aspects and Relation to Circadian Rhythm

The function of ultradian rhythms is not yet clearly elucidated. In particular, short-term rhythms are expressed during early ontogeny, especially in broods of precocial birds. We investigated the relationship between the clarity of the ultradian rhythm of the activity/rest cycle of a group of young Japanese quail (Coturnix japonica) and the level of social synchronisation and spatial cohesion between the birds within that group. The subjects were descended from two lines selected for either very pronounced rhythmic or arrhythmic circadian activity. We found a positive relationship between the clarity of the ultradian rhythm of the activity/rest cycle when birds were young and the clarity of the circadian rhythm of feeding activity when birds were older, but still immature. The temporal organisation of the behaviour of the chicks from these two lines was observed in outdoor aviaries, when they were 4, 8, 12 and 15 days old. The mean ultradian period expressed by groups of 12 chicks was variable, with a minimum of 6 minutes. The ultradian period lengthened regularly as chicks grew older, and reached approximately 40 min on day 15. The clarity of the ultradian rhythmicity of group activity was linked to the level of inter-individual social synchronisation and of spatial cohesion; the more pronounced the ultradian rhythms of a group, the greater the temporal and spatial cohesion of the chicks within the group. Moreover, these characteristics varied with the age of the chicks. Finally, chicks in the less rhythmic groups weighed less. These results stress the adaptive value of this temporal organisation strategy under natural conditions.     

Effects of an acute stressor on fear and on the social reinstatement responses of domestic chicks to cagemates and strangers

Genetic selection for appropriate levels of sociality (motivation to be with conspecifics) could benefit poultry welfare and performance. Runway tests that require chicks to traverse a corridor in order to reach other chicks in a goal box are commonly used to measure this behavioural trait. However, we need to determine if the chicks' responses in such tests are sensitive to certain experiential variables before we can recommend possible selection criteria for future breeding programmes. The present study focused on fear and on the identity of the stimulus birds. Broiler chicks either remained undisturbed or were exposed to an acute stressor (mechanical restraint) before their tonic immobility fear responses were measured 1h later in Experiment 1. Exposure to the stressor significantly prolonged tonic immobility and, hence, presumably, underlying fear levels. In Experiment 2, the responses of stressed chicks and undisturbed controls were assessed when they were tested individually in a runway with a goal box containing either familiar or unfamiliar chicks of the same age. Our finding that stressed chicks emerged from the start box sooner and spent longer near the stimulus birds suggests that exposure to a frightening event increased social reinstatement motivation. Furthermore, social affiliation was more pronounced when the goal box contained familiar cagemates rather than strange chicks, regardless of prior treatment. This finding demonstrates that broiler chicks that were housed in groups of twelve can discriminate between familiar and unfamiliar conspecifics encountered in novel surroundings. Thus, sociality was positively associated with fearfulness and broilers clearly showed social discrimination in runway tests. These findings highlight the dangers of disregarding variables, such as fear and the capacity for social recognition in tests of social motivation. We strongly recommend that exposure to frightening events prior to test should be avoided and that the identity of the birds in the runway goal box should be standardized, i.e. either familiar or unfamiliar, and noted.     

Synchronization of Ultradian Rhythms of Activity in Young Japanese Quail: Effect of Kin Relationships

Synchronization of activity cycles is common in coveys of gallinaceous birds, which usually include a dozen chicks at birth. To study this synchronization more precisely, we recorded the ultradian rhythms of activity of seven groups of young Japanese quail reared in the laboratory, without brooding females. Four groups included only kin-related birds (K1-K4), two mixed groups consisted of associated chicks from two families (M1 and M2 groups), and the seventh group (NK group) included only non-kin chicks. Numbers of chicks in a group varied from eight to 14, depending on the group. They were observed twice during their two first weeks of life (day 3 and day 10) and all activities were recorded by scan sampling. An ultradian rhythm of activity, with a period less than 20 minutes, was found. This period varied among quail families. All chick groups were globally synchronized, except group M2 on day 3. Inter-individual levels of synchronization were calculated. Spearman rank correlation coefficients of the non-kin chicks were significantly lower than those of kin-related chicks. This was especially clear on day 3. Survival of newborn quails is linked to their presence within a covey or a group. Their survival, as well that of their brothers and sisters, may be enhanced by an ability to synchronize with kin better than with non-kin chicks.     

Maternal presence influences vocal development in the Japanese quail (Coturnix c. japonica)

Social influences on vocal development of young birds have been widely studied in oscine songbirds who learn to sing by vocal imitation of conspecifics, mainly male adults. In contrast, vocal development of non-vocal learners such as Galliformes is considered as being under strong genetic influence and independent of the social environment. In this study, we investigated the role of the mother on the vocal development of young Japanese quail (Coturnix coturnix japonica). We compared the vocal development of mothered and non-mothered chicks during the first 21 days of life. We analysed the structural changes of two vocalisations: a) the rally call, emitted during long-distance communication and in stressful situations, b) the contact call, emitted during short-distance communication when chicks are in visual and/or auditory contact with congeners. We showed that temporal and spectral structures of the two types of calls changed during development and differed between mothered and non-mothered chicks. These results demonstrate that maternal presence influences the vocal development of the young in the Japanese quail. Even if the adaptive value of such changes was not assessed, these results highlight that plasticity of vocalisations in species considered as non-vocal learners has been underestimated.     

Age of the incubating parents affects nestling survival: an experimental study of the herring gull Larus argentatus

The quality of conditions provided by avian parents will have consequences for both parental and offspring fitness. While many components of avian reproduction appear to vary with parental age, the effect of age on incubation has largely been ignored so far. In this study, we tested whether young herring gulls provide a different incubation environment from mature ones and whether this has consequences for offspring performance. Laying and rearing conditions were standardised using a cross-fostering protocol. Egg predation rates tended to be higher in the nests of young parents. However, nest site, nest construction and egg temperature during incubation did not vary with parental age. Overall, the duration of incubation was shorter in young compared to mature birds and this reflected the later laying date of the former, since incubation duration generally decreased across the season. However, male eggs incubated by young parents had longer incubation periods than predicted for their laying dates. In contrast, incubation length of female eggs incubated by young pairs, and of male and female eggs incubated by mature birds did not deviate from the expected for any given laying date. Offspring that had been incubated by young parents had considerably poorer survival than those incubated by mature pairs, despite being reared under standardized, favourable conditions (singly, by mature parents). This was due to increased mortality among female chicks that had been incubated by young parents. The chicks incubated as eggs by young and mature birds, which survived until fledging, did not differ in body mass and size growth, or body condition. The results of this study demonstrate that parental age can influence offspring performance via variation in incubation environment, and that females are more susceptible than males to conditions experienced during embryonic development.     

Effects of ectoparasites of young on parents' behaviour in a Mediterranean population of Blue Tits

In altricial birds, adults are expected to alleviate the impact of parasitism on their young by increasing parental care. We experimentally investigated the effects of blowfly parasitism on adult behaviour in the nest cavity in a population of Blue Tits in which nestlings are heavily parasitized by blowfly larvae. The behaviour of males and females was different, since only the females carried out nest sanitation activities related to the presence of parasites. The time females devoted to nest sanitation was higher in parasitized nests than in experimentally deparasitized ones, suggesting that chicks and adults might share the costs of blowfly parasitism.     

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.