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Experience modulates emission of food calls in broody hens
C.R. Acad. Sci. Paris, Sciences de la vie / Life Sciences 324 (2001) 1021–1027 © 2001 Académie des Sciences/Éditions scientifiques et médicales Elsevier SAS. Tous droits réservés S0764446901013622/FLA
Écologie/ecology
Experience modulates emission of food calls in broody hens Aline-Marie Wauters, Marie-Annick Richard-Yris* UMR CNRS-6552, éthologie–évolution–écologie, université Rennes-I, campus de Beaulieu, av. Gén. Leclerc, 35042 Rennes cedex, France Received 19 February 2001; accepted 3 May 2001 Communicated by Jean Pierre Dorst
Abstract – The aim of these experiments was to determine if previous experience of chicks’ response to food calling influences subsequent propension of maternal hens to utter food calls. Seventeen broody hens were tested three times a day without their 3- or 4-day-old chicks. Hens were tested in two situations: chicks were returned either after each test or at the end of all the day’s tests. As palatability influences food calling in maternal hens, experiments were conducted first with a highly preferred food item and then with the hens’ usual feed. The chicks’ capacity to respond regularly to their mother influences the hens’ capacity to emit food calls. In fact, although the hens did not lose their maternal state, they uttered fewer food calls when their chicks were removed all day. These results suggest that the chicks’ behaviour following food calling could be a social reinforcement for broody hens. © 2001 Académie des Sciences/Éditions scientifiques et médicales Elsevier SAS food call / experience / maternal behaviour / Gallus gallus domesticus
Résumé – L’expérience de la poule maternelle module son taux d’émission du cri d’offrande alimentaire. Ces expériences ont pour but de déterminer si l’émission soutenue de cris d’offrande par des poules maternelles dépend de l’expérience liée aux réponses des jeunes aux cris de leur mère en dehors des tests. Dix-sept poules maternelles reçoivent trois tests par jour en l’absence de leurs jeunes âgés de trois et quatre jours. Hors test, deux situations sont utilisées : soit les poussins sont présents, soit ils sont absents. Un aliment très appétant est présenté en test pendant l’expérience 1, un aliment habituel pendant l’expérience 2. Quel que soit l’aliment, la capacité des poussins à répondre régulièrement aux vocalisations des mères favorise la production des cris. Lorsque les jeunes ne peuvent pas répondre aux cris, les poules, quoique toujours maternelles, émettent moins de cris. Ces résultats suggèrent que les comportements émis par les poussins en réponse aux cris d’offrande des mères puissent constituer un puissant renforçateur social pour les poules. © 2001 Académie des Sciences/Éditions scientifiques et médicales Elsevier SAS cri d’offrande alimentaire / expérience / comportement maternel / Gallus gallus domesticus
. Version abrégée Chez de nombreuses espèces sociales d’oiseaux et de primates, il existe des vocalisations particulières
nommées « cris associés à la nourriture » ou « cris d’offrande alimentaire ». Chez les oiseaux, les études les plus développées sur les cris d’offrande alimentaire concernent les poulets sauvages et domestiques. Dans
*Correspondence and reprints. E-mail address: [email protected] (M.A. Richard-Yris).
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A.-M. Wauters, M.-A. Richard-Yris / C.R. Acad. Sci. Paris, Sciences de la vie / Life Sciences 324 (2001) 1021–1027
le cas des poulets, des études descriptives ont montré que la vocalisation était principalement émise par les coqs adultes et les poules maternelles. L’émission de la vocalisation induit l’approche des individus de la même espèce vers le lieu de l’émission. Ainsi, les cris d’offrande d’un coq attirent les femelles à son voisinage tandis que les cris d’offrande de la mère poule attirent ses poussins autour de son bec. L’émission des vocalisations d’offrande a souvent été interprétée par les auteurs comme indiquant l’existence de processus cognitifs complexes comme l’intentionnalité de l’émetteur. Chez la poule maternelle comme chez le coq, divers travaux ont montré l’existence d’un lien entre le contexte alimentaire et la production du cri. De même, plusieurs études soulignent l’influence du contexte social sur la tendance des animaux à émettre le cri d’offrande. Ainsi, en présence d’aliments, une poule maternelle produit davantage de vocalisations lorsque ses petits n’ont pas accès à la nourriture ou lorsqu’ils sont séparés d’elle pour quelques instants. L’expérience de l’émetteur semble également importante à considérer puisque lors d’une procédure de conditionnement avec signal avertisseur lumineux, des coqs adultes sont capables d’émettre des cris d’offrande dès que la lampe annonçant l’arrivée prochaine de l’aliment s’allume dans la cage. Par contre, jusqu’à présent les auteurs se sont peu intéressés à l’impact que peuvent avoir les réponses du receveur sur la production du cri. Ainsi, on sait que chez les poules maternelles, l’émission du cri d’offrande diminue et même cesse dès que les petits ont rejoint leur mère, après qu’elle a crié, et picorent avec elle. Au contraire, l’émission des cris est plus importante s’ils tardent à la rejoindre. Il est donc possible que la poule associe par simple conditionnement sa production vocale avec une approche plus ou moins rapide des poussins. Cette hypothèse implique qu’une absence prolongée des comportements d’approche et de picorage des jeunes qui suivent normalement l’émission du cri d’offrande de la mère, peut induire un déclin de la propension de la mère à émettre un nombre important de cris. C’est cette hypothèse que nous avons souhaité tester en recherchant si la possibilité pour les poussins de répondre régulièrement aux cris de leur mère pouvait constituer un renforcement de la tendance de celle-ci à émettre de nombreux cris en l’absence des jeunes. En d’autres termes, nous avons cherché à savoir si l’émission du cri d’offrande était sensible à un conditionnement contextuel à renforcement social, lié à l’histoire de l’émetteur. Dans ce but, nous avons effectué successivement deux expériences avec dix-sept poules maternelles et leurs deux poussins. Quelle que soit l’expérience, durant les deux premiers jours de vie des jeunes, chaque poule reste en présence continuelle de ses jeunes dans une cage où le groupe mère–jeunes dispose d’aliments
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(blé + aliment démarrage poussins) et d’eau à volonté. Par ailleurs, strictement identiques du point de vue du protocole, les deux expériences diffèrent par l’aliment utilisé lors des tests. L’appétence des aliments étant susceptible de moduler l’émission du cri d’offrande, les poules ont été testées soit avec un aliment hautement préféré (une bouillie constituée de granulés et d’eau surmontée de cinq vers de farine) (expérience 1), soit avec l’aliment habituel (expérience 2). Lors de chaque expérience, les poules sont testées trois fois par jour lorsque les jeunes ont trois et quatre jours. Chaque test consiste à présenter à chaque poule un aliment pendant 3 min en l’absence des poussins. Les poules sont testées dans deux situations : – en situation A, les poules restent avec leurs poussins sauf au moment des tests. La séparation mère–jeunes intervient 2 min avant chaque test et se termine après les 3 min du test. – en situation B, les poules sont séparées de leurs jeunes le matin du jour des tests, 30 min avant le premier test. Le retour des poussins n’est permis qu’à l’issue du dernier test de la journée. Durant chaque test, on mesure le nombre de cris d’offrande émis et le taux d’activité alimentaire de la poule estimé par le nombre de périodes de 15 s pendant lesquelles la poule picore. Les résultats montrent que bien que le nombre de cris d’offrande émis par les poules soit plus élevé en présence de l’aliment très appétant que vis-à-vis de l’aliment habituel, l’impact de la présence ou de l’absence des jeunes hors de la situation de test module bien l’émission du cri d’offrande. En effet, dans la situation A, où les poussins peuvent répondre par des comportements d’approche aux cris que leurs mères émettent sur la mangeoire habituelle, le nombre des cris d’offrande émis en situation de test est significativement supérieur à celui qu’elles émettent quand cette possibilité n’est pas permise. Dans le cas où les poules peuvent interagir avec leurs jeunes (situation A), les mères continuent à expérimenter le lien de contiguïté temporelle entre l’émission du cri d’offrande, l’approche et le picorage de leurs jeunes. Ce comportement des petits pourrait alors constituer un renforcement social pour les mères. Dans le cas où les poules sont privées de leurs jeunes toute la journée, comme dans la situation B, elles se trouveraient en phase d’extinction prolongée puisque leurs émissions de cris d’offrande sur la mangeoire habituelle ou de test ne sont suivies d’aucune réponse. Ceci pourrait expliquer que, bien qu’étant toujours maternelles, les poules émettent moins de cris d’offrande dans ce cas. Cette hypothèse est d’autant plus probable que divers auteurs comme Guyomarc’h ou Moffatt et Hogan ont mis en évidence de telles capacités d’apprentissage simple chez les poussins. L’hypothèse de l’existence de pro-
A.-M. Wauters, M.-A. Richard-Yris / C.R. Acad. Sci. Paris, Sciences de la vie / Life Sciences 324 (2001) 1021–1027
cessus complexes comme l’intentionnalité ne semble donc pas nécessaire pour interpréter les résultats obtenus dans notre étude. L’intervention d’une forme simple
de conditionnement permet une interprétation plus parcimonieuse des résultats obtenus.
1. Introduction
food calls they emitted [16]. Moreover, in the presence of their usual diet, hunger level positively affected food call production [16]. In addition, food calling in maternal hens is modulated by the caller’s social context: presence of chicks, behaviour of chicks and separation from chicks modified food call production [12, 27, 28]: for example, when food was present, hens uttered longer when chicks were in the same cage but did not have access to the food, than when they could approach the food and feed nearby [28]. Moreover, in the presence of food items, hens produced more food calls in the temporary absence of chicks than in their presence [16]. Similarly, when chicks were separated from their mother, who could still hear and see them, maternal hens uttered more food calls than when chicks were free in the same cage [28]. These data coincide with observations made under natural conditions by Stokes [6]. He observed that hens’ food calls became louder, faster and longer with increasing distance between hen and chicks as chicks mature. Therefore, in the presence of food, hens appeared to utter more food calls when their chicks were too far away and more generally when the chicks did not respond to their calls by going toward their mother’s head to eat. To explain the modulation of food call production, a straightforward hypothesis would be that hens could associate, by simple conditioning, their vocal production with the more or less rapid approach of chicks. This hypothesis implies that the repeated absence of approach and pecking of chicks following food calls induces a decline of the hen’s tendency to utter many food calls in the presence of palatable food items. In this study, we investigated whether the possibility for chicks to respond regularly to their mother’s calls could reinforce the hen’s tendency to utter many food calls when her chicks are temporarily absent. In other words, we investigated whether food calling is sensitive to ‘historical’ contextual conditioning with filial reinforcement [29].
Food associated calls have been reported in several primate species [1, for review] and in a number of bird species, including gallinaceous birds [2–7], common ravens [8], house sparrows [9] and cliff swallows [10]. Sound spectrograms reveal that the food calls of both domestic and red junglefowl chickens consist of a series of pulse-like sounds delivered at almost regular intervals [11–13]. These rhythmically repeated calls were generally uttered when a bird was frequently picking up and dropping either edible or inedible objects, that, usually, it did not swallow [4]. Descriptive studies indicate that food calls are usually produced by cockerels and broody hens with chicks, but are sometimes emitted by non broody hens [14–16] and more rarely by chicks [17]. Several studies reported that food calling cockerels attract hens to their vicinity [18] and food calling maternal hens attract chicks to the mother’s beak [12]. The study of Evans and Evans [19] supports the hypothesis of a functional reference for food calls, as signals with the property of functional reference should be sufficient, in the absence of eliciting stimuli and of other normally available cues, to permit receivers to select appropriate responses [25, 26]. The most detailed studies of food calls concern male chickens [20–24]. Male food calls appear to be induced by food items and by stimuli that predict reliably the availability of food [23]. Some studies also revealed that the rate at which males produce food calls reflects their preference for a given food stimulus, so that it is higher for living mealworms than for less preferred items like their regular rations [20]. Other experiments revealed a social dimension of male food calls: cockerels uttered significantly more food calls when a hen was confined in an adjacent cage than when they were alone [21, 23] or when another male was present [21]. Nevertheless these observations raised two problems. First, the almost absence of emission when another male is present can be explained differently in function of the type of information (simply ‘food’ or ‘food and propensity to share it’) carried by the signal. The second problem is that, during tests, each male was separated from his familiar female. The absence of a response from the receiver (the hen), more than its simple presence, could be at the origin of the higher food call rate. Furthermore, food calling is sensitive to contextual conditioning: food calling in the absence of a female increased after training in her presence and decreased again after training in her absence [15]. Maternal hens also modulate their production of food calls in relation to the quality of the food they have found: the more the maternal hens preferred a food type, the more
2. Material and methods 2.1. Subjects
Seventeen two-year-old domestic hens from a commercial meat-strain (‘Elevage Gauguet’) were housed in individual wire-mesh cages (100 × 70 × 60 cm) with opaque lateral partitions and nest-boxes. Thus, each bird was isolated visually but not auditorily from the others. Birds were maintained under a constant artificial photoperiod (14L:10D); temperature of the experimental room was 20 ± 2 °C. Apart from a short period of food restriction, all animals were provided with water and a mixture of whole wheat and commercial diet at libitum.
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2.2. Induction of maternal behaviour
To induce maternal behaviour, laying hens were deprived of food for 2 days and then were given only restricted rations (50 g·bird–1·day–1) of whole wheat for the following 6 days in order to stop egg laying and to ensure rapid onset of maternal responses [30]. This method, routinely used in our laboratory, may appear severe but no ill effects have even been recorded following this treatment (weight loss = 5 %). Thereafter, food was provided ad libitum. Maternal behaviour was experimentally induced 2 days after the end of the food-restriction period: the hens were shut in their nest-boxes at lights out, and 2 h later two newly hatched chicks were gently placed under each hen. The doors of the nest-boxes were removed the following morning, 30 min before the lights came on, to allow access to the entire cage. All hens giving chicks following this procedure accepted them and showed complete brooding behaviour with clucking and food calls. These chicks remained with their foster mother for 7 days and were then replaced by the newly hatched chicks used in experiment 1. When chicks were 8 days old, they were replaced by the newly hatched chicks used in experiment 2. 2.3. Test procedure
Two successive experiments (experiments 1 and 2) were conducted, using two types of food. As food palatability can influence food calling in maternal hens [16], experiments were first conducted with a highly preferred food item (experiment 1), and then, with the hens’ usual feed (experiment 2). For these experiments, the same hens were used with two different batches of chicks. During each experiment, broody hens were tested three times a day when their chicks were 3 and 4 days old. A test consisted in presenting a dish with food for 3 min in the hen’s home-cage. The tests were always carried out in the chicks’ absence. They started 1 h 30 after lights-on and were replicated 3 times during the day, at an interval of 3 h. The hens were tested in two different situations: – Situation A: the hens were with chicks all the time except during the tests. The chicks were removed, from their cage 2 min before each test and placed in a distant, heated room. They were returned to their mother’s cage after each 3-min test. – Situation B: the chicks were removed from their mother’s cage 30 min before the first test and were returned only 15 min after the last test of the day. To ensure that the hens were presented to the same experimenter-effect in the two situations, in the situation B the observer opened the cage and placed her hands in it as many times as she had to do it in situation A. Eight hens were tested in situation A when the chicks were 3 days old and in situation B the next day, when the chicks were 4 days old. The other nine hens were tested in the reverse order.
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Each test began when a transparent plastic dish (9 cm in diameter, 5 cm deep), fixed onto a small piece of wood, was introduced into the cage. In experiment 1, each hen was presented a highly preferred food item called ‘wormmash’ [16]: 5 mealworms on 50 g of wet mash (25 g of pellets and 25 g of water). In experiment 2, each hen was presented 50 g of a mixture of whole wheat and commercial ‘starter’ diet called ‘usual feed’. During the 3-min test the following measures were recorded: – The quantity of a hen’s feeding activity was estimated by the number of 15-s periods when it was observed. – The number of food calls for each 15-s period. Food calls were easily identified by ear and were counted directly as the observer heard them. At the same time, the vocalizations were tape-recorded and were blindly counted again after each observation. A microphone -LEM EMU4535-, connected to a tape-recorder -Marentz CP430-, was used to record vocalizations. Observations and vocalization recordings ended after 3 min. However, in all cases, after a test, the food dish was left in the cage for 3 more min. As the hens tested in situation A were reunited with their chicks at the end of each 3-min test, they had the possibility to see their chicks respond to their food calls by pecking in the dish, a reaction they otherwise experience all the time when they utter food calls at their usual feeding trough. The maintenance of the maternal state of hens was tested after the end of the last test of the day by recording their behaviour: a hen that clucked, food called and accepted the chicks under her when they were returned to their mother’s cage was considered to be maternal. 2.4. Statistical analyses
For each experiment, i.e., for each type of food presented, the data were analysed using a repeated-measures ANOVA with factors for test situation (A or B) and test number (1, 2 or 3), followed, if appropriate (P < 0.05), by further post hoc analysis using Student paired t-tests and Bonferroni–Dunn tests.
3. Results In situation B, as in situation A, all hens uttered clucks, food calls and accepted their young under them after the last test of the day, indicating that they were still maternal. Although maternal hens uttered significantly more food calls in the presence of their preferred food (worm-mash) than in the presence of their usual feed, in both cases the possibility to interact or not with chicks influenced the number of food calls uttered during tests (figure 1). Hens, in situation B, when chicks were removed all day, uttered significantly (P < 0.0001) fewer food calls after the first test than in situation A when chicks were returned to their mother immediately after each test. As in other experiments [16], we obtained a similar result when only the number of 15-s periods were considered (P < 0.008).
A.-M. Wauters, M.-A. Richard-Yris / C.R. Acad. Sci. Paris, Sciences de la vie / Life Sciences 324 (2001) 1021–1027
Table I. Pecking during tests.
percentage of 15-s periods
Test 1
during which hens pecked (Mean ± SE)
Test 2
Test 3
M
SE
M
SE
M
Se
Wet mash + mealworms brief separation (A) continuous separation (B)
92.2 95.6
4.3 3.4
96.6 91.2
2.4 3.8
90.7 84.8
3.7 5.7
Wheat / commercial ‘starter diet’ brief separation (A) continuous separation (B)
90.7 90.7
4.2 5.1
80.4 74.0
8.1 7.9
82.8 93.1
8.7 3.7
4. Discussion
Figure 1. Food Calling by Maternal Hens during Tests. In situation A , chicks were returned to their mother after each 3 min test; in situation B , hens remained alone all day. N: mean number of food calls emitted during a test. *: significant differences between situations for each test (Student paired t-test, n = 17, p < 0.05). a: significant differences (p < 0.05) between test 1 and other tests for each situation (Bonferroni–Dunn post hoc test, n = 17).
In the presence of their preferred food as well as in the presence of their usual feed, the hen’s capacity to utter food calls varied in relation to test number (Bonferroni–Dunn, P < 0.05) (table I, figure 1): the number of food calls decreased with time. On the other hand, pecking, estimated by the number of 15-s periods when hens pecked, did not vary significantly with test number (P > 0.05) (table I).
Data presented here confirm that maternal hens are able to utter food calls in the presence of food even in the absence of their chicks [12, 16, 28]. In addition, when a hen always remained with her chicks that were only removed during the short time each test lasted (situation A), she uttered significantly more food calls than when mother-chick separation lasted longer and began 30 min before the first test. In situation A, hens could interact freely with their chicks all day long. This constant presence alone could maintain a strong tendency in the hen to utter food calls during the tests. Similarly, Sherry [12] observed that hens presented with a mealworm produced food calls for longer just after they had been separated from their young than when they could see them. He suggested that this call may also be used by the hen to gather her brood. The underlying idea suggested by this author is that this call is used intentionally by hens to attract their chicks. However, this interpretation does not seem to be sustained by some other observations. Indeed, if this was a hard and fast rule, we could suppose that hens temporarily deprived of their chicks would also utter many food calls when food is absent or not very palatable. However, this does not seem to be the case because, when no food was present during a test, isolated hens uttered very few food calls or none at all [28]. Another interpretation can be done if we refer to the behaviour of chicks reared in natural conditions. When chicks can interact freely with their mother, they generally respond by approaching her rapidly and pecking each time the hen utters food calls [17]. No doubt hens are able to learn that their food calls are nearly always followed by the approach of their chicks. This associated approach and/or pecking by chicks could be a social reinforcement for the hens. When they have been deprived of their chicks for several hours, like in situation B, the hens would be in a state of prolonged extinction insofar as their food calls uttered when they were pecking in the feeding trough were not followed by any response. This could explain why, in this situation, hens, that were still maternal, uttered fewer food calls than in situation A. Several authors have shown that chickens possess similar simple learning capacities. Guyomarc’h [31] showed that chicks learned, through
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simple conditioning, the semantic value of the hen’s food call. Similarly, Moffatt and Hogan [32] showed that although 5-day-old chicks have a prefunctional tendency to respond more readily to faster than to slower rates of food calls, this tendency could be modified by experience. Evans and Marler [23] showed that food calling by cockerels is not limited to edible food items but that it is also associated with stimuli that have, in the past, reliably predicted the presence of food. In addition, maternal hens that had only seen their chicks during daytime (12 days ago) produced fewer food calls in a test when chicks were free, than other maternal hens [33]. The authors hypothesized that hens, that had only seen chicks, had never experienced complete approach responses following food calls during these 12 days because they were separated from chicks and this could explain why these hens subsequently emitted fewer food calls during a test. Each individual historical context would therefore be liable to modulate the quantity of food calls that a maternal hen is likely to utter in the presence of food. On the other hand, in the experiment described here the number of food calls uttered decreased with test number regardless of food type. It is as if replication of the same test conditions during the same day induced a reduction of the hen’s tendency to utter many food calls. A similar tendency was described by Sherry [12] concerning daily tests in the absence of chicks. Even though we have no definite explanation of this decline, we can suggest several hypoth-
eses. Under our experimental conditions, three tests were conducted during the same day and the hens had permanent access to food in their home cage. The decline in the number of food calls recorded could possibly be the result of a decline in interest for the food presented in relation to the animals’ hunger level, as their hunger necessarily decreased between test 1 and test 3. Hunger level is known to modulate the quantity of food calls uttered by cockerels [23] as well as by hens [16]. Nevertheless, it must be remembered that pecking, estimated by the number of 15-s periods when pecking in the dish was observed, did not vary significantly with test number. In addition, the effect of the time of day when the food test was presented must not be dismissed. This greater tendency to food call in the morning has also been reported in primates [34, 35] and could be due to fasting during the night, but also to ultradian feeding or arousal rhythms. Finally, food calling in most gallinaceous birds is known to be stimulated by uncommon food items [4, 6, 14, 16]. Replicate presentations during the same day of the same food type could induce a decline of its relative novelty which seems to stimulate the emission of a greater number of food calls.
References
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To conclude, the supposed existence of complex cognitive processuses, as intentionality, is not necessary to interpret the obtained results. These results rather form a possible role of the operant conditioning in the development of a naturaly occuring communication behaviour.
A.-M. Wauters, M.-A. Richard-Yris / C.R. Acad. Sci. Paris, Sciences de la vie / Life Sciences 324 (2001) 1021–1027 [27] Hughes M.K., Hughes A.L., Covalt-Dunning D., Stimuli eliciting foodcalling in domestic chickens, Appl. Anim. Ethol. 8 (1982) 543–550. [28] Wauters A.M., Richard-Yris M.A., Pierre J.S., Lunel C., Richard J.P., Influence of chicks and food quality on food calling in broody domestic hens, Behaviour 136 (1999) 919–933. [29] Smith W.J., Animal communication and the study of cognition, in: Ristau C.A. (Ed.), Cognitive Ethology. Hilsdale, Laurence Erlbaum, NewJersey, 1991, pp. 209–229. [30] Richard-Yris M.A., Chikhi L., Maternal behaviour in domestic hens (Gallus gallus domesticus): cues from chicks and maintenance of maternal responsiveness, Int. J. Comp. Psychol. 4 (1991) 275–286. [31] Guyomarc’h J.C., Le rôle de l’expérience sur la sémantique du cri d’offrande alimentaire chez le poussin, Rev. Comport. Anim. 9 (1974) 219–236.
[32] Moffatt C.A., Hogan J.A., Ontogeny of chick responses to maternal food calls in the Burmese red junglefowl (Gallus gallus spadiceus), J. Comp. Physiol. 106 (1992) 92–96. [33] Richard-Yris M.A., Garnier D.H., Leboucher G., Induction of maternal behavior and some hormonal and physiological correlates in the domestic hen, Horm. Behav. 17 (1983) 345–355. [34] Hauser M.D., Marler P., Food-associated calls in rhesus Macaques (Macaca mulatta): I- Socioecological factors, Behav. Ecol. 4 (1993) 194–205. [35] Hauser M.D., Marler P., Food-associated calls in rhesus Macaques (Macaca mulatta): II- Costs and benefits of call production and suppression, Behav. Ecol. 4 (1993) 206–212.
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Écologie/ecology
Experience modulates emission of food calls in broody hens Aline-Marie Wauters, Marie-Annick Richard-Yris* UMR CNRS-6552, éthologie–évolution–écologie, université Rennes-I, campus de Beaulieu, av. Gén. Leclerc, 35042 Rennes cedex, France Received 19 February 2001; accepted 3 May 2001 Communicated by Jean Pierre Dorst
Abstract – The aim of these experiments was to determine if previous experience of chicks’ response to food calling influences subsequent propension of maternal hens to utter food calls. Seventeen broody hens were tested three times a day without their 3- or 4-day-old chicks. Hens were tested in two situations: chicks were returned either after each test or at the end of all the day’s tests. As palatability influences food calling in maternal hens, experiments were conducted first with a highly preferred food item and then with the hens’ usual feed. The chicks’ capacity to respond regularly to their mother influences the hens’ capacity to emit food calls. In fact, although the hens did not lose their maternal state, they uttered fewer food calls when their chicks were removed all day. These results suggest that the chicks’ behaviour following food calling could be a social reinforcement for broody hens. © 2001 Académie des Sciences/Éditions scientifiques et médicales Elsevier SAS food call / experience / maternal behaviour / Gallus gallus domesticus
Résumé – L’expérience de la poule maternelle module son taux d’émission du cri d’offrande alimentaire. Ces expériences ont pour but de déterminer si l’émission soutenue de cris d’offrande par des poules maternelles dépend de l’expérience liée aux réponses des jeunes aux cris de leur mère en dehors des tests. Dix-sept poules maternelles reçoivent trois tests par jour en l’absence de leurs jeunes âgés de trois et quatre jours. Hors test, deux situations sont utilisées : soit les poussins sont présents, soit ils sont absents. Un aliment très appétant est présenté en test pendant l’expérience 1, un aliment habituel pendant l’expérience 2. Quel que soit l’aliment, la capacité des poussins à répondre régulièrement aux vocalisations des mères favorise la production des cris. Lorsque les jeunes ne peuvent pas répondre aux cris, les poules, quoique toujours maternelles, émettent moins de cris. Ces résultats suggèrent que les comportements émis par les poussins en réponse aux cris d’offrande des mères puissent constituer un puissant renforçateur social pour les poules. © 2001 Académie des Sciences/Éditions scientifiques et médicales Elsevier SAS cri d’offrande alimentaire / expérience / comportement maternel / Gallus gallus domesticus
. Version abrégée Chez de nombreuses espèces sociales d’oiseaux et de primates, il existe des vocalisations particulières
nommées « cris associés à la nourriture » ou « cris d’offrande alimentaire ». Chez les oiseaux, les études les plus développées sur les cris d’offrande alimentaire concernent les poulets sauvages et domestiques. Dans
*Correspondence and reprints. E-mail address: [email protected] (M.A. Richard-Yris).
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A.-M. Wauters, M.-A. Richard-Yris / C.R. Acad. Sci. Paris, Sciences de la vie / Life Sciences 324 (2001) 1021–1027
le cas des poulets, des études descriptives ont montré que la vocalisation était principalement émise par les coqs adultes et les poules maternelles. L’émission de la vocalisation induit l’approche des individus de la même espèce vers le lieu de l’émission. Ainsi, les cris d’offrande d’un coq attirent les femelles à son voisinage tandis que les cris d’offrande de la mère poule attirent ses poussins autour de son bec. L’émission des vocalisations d’offrande a souvent été interprétée par les auteurs comme indiquant l’existence de processus cognitifs complexes comme l’intentionnalité de l’émetteur. Chez la poule maternelle comme chez le coq, divers travaux ont montré l’existence d’un lien entre le contexte alimentaire et la production du cri. De même, plusieurs études soulignent l’influence du contexte social sur la tendance des animaux à émettre le cri d’offrande. Ainsi, en présence d’aliments, une poule maternelle produit davantage de vocalisations lorsque ses petits n’ont pas accès à la nourriture ou lorsqu’ils sont séparés d’elle pour quelques instants. L’expérience de l’émetteur semble également importante à considérer puisque lors d’une procédure de conditionnement avec signal avertisseur lumineux, des coqs adultes sont capables d’émettre des cris d’offrande dès que la lampe annonçant l’arrivée prochaine de l’aliment s’allume dans la cage. Par contre, jusqu’à présent les auteurs se sont peu intéressés à l’impact que peuvent avoir les réponses du receveur sur la production du cri. Ainsi, on sait que chez les poules maternelles, l’émission du cri d’offrande diminue et même cesse dès que les petits ont rejoint leur mère, après qu’elle a crié, et picorent avec elle. Au contraire, l’émission des cris est plus importante s’ils tardent à la rejoindre. Il est donc possible que la poule associe par simple conditionnement sa production vocale avec une approche plus ou moins rapide des poussins. Cette hypothèse implique qu’une absence prolongée des comportements d’approche et de picorage des jeunes qui suivent normalement l’émission du cri d’offrande de la mère, peut induire un déclin de la propension de la mère à émettre un nombre important de cris. C’est cette hypothèse que nous avons souhaité tester en recherchant si la possibilité pour les poussins de répondre régulièrement aux cris de leur mère pouvait constituer un renforcement de la tendance de celle-ci à émettre de nombreux cris en l’absence des jeunes. En d’autres termes, nous avons cherché à savoir si l’émission du cri d’offrande était sensible à un conditionnement contextuel à renforcement social, lié à l’histoire de l’émetteur. Dans ce but, nous avons effectué successivement deux expériences avec dix-sept poules maternelles et leurs deux poussins. Quelle que soit l’expérience, durant les deux premiers jours de vie des jeunes, chaque poule reste en présence continuelle de ses jeunes dans une cage où le groupe mère–jeunes dispose d’aliments
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(blé + aliment démarrage poussins) et d’eau à volonté. Par ailleurs, strictement identiques du point de vue du protocole, les deux expériences diffèrent par l’aliment utilisé lors des tests. L’appétence des aliments étant susceptible de moduler l’émission du cri d’offrande, les poules ont été testées soit avec un aliment hautement préféré (une bouillie constituée de granulés et d’eau surmontée de cinq vers de farine) (expérience 1), soit avec l’aliment habituel (expérience 2). Lors de chaque expérience, les poules sont testées trois fois par jour lorsque les jeunes ont trois et quatre jours. Chaque test consiste à présenter à chaque poule un aliment pendant 3 min en l’absence des poussins. Les poules sont testées dans deux situations : – en situation A, les poules restent avec leurs poussins sauf au moment des tests. La séparation mère–jeunes intervient 2 min avant chaque test et se termine après les 3 min du test. – en situation B, les poules sont séparées de leurs jeunes le matin du jour des tests, 30 min avant le premier test. Le retour des poussins n’est permis qu’à l’issue du dernier test de la journée. Durant chaque test, on mesure le nombre de cris d’offrande émis et le taux d’activité alimentaire de la poule estimé par le nombre de périodes de 15 s pendant lesquelles la poule picore. Les résultats montrent que bien que le nombre de cris d’offrande émis par les poules soit plus élevé en présence de l’aliment très appétant que vis-à-vis de l’aliment habituel, l’impact de la présence ou de l’absence des jeunes hors de la situation de test module bien l’émission du cri d’offrande. En effet, dans la situation A, où les poussins peuvent répondre par des comportements d’approche aux cris que leurs mères émettent sur la mangeoire habituelle, le nombre des cris d’offrande émis en situation de test est significativement supérieur à celui qu’elles émettent quand cette possibilité n’est pas permise. Dans le cas où les poules peuvent interagir avec leurs jeunes (situation A), les mères continuent à expérimenter le lien de contiguïté temporelle entre l’émission du cri d’offrande, l’approche et le picorage de leurs jeunes. Ce comportement des petits pourrait alors constituer un renforcement social pour les mères. Dans le cas où les poules sont privées de leurs jeunes toute la journée, comme dans la situation B, elles se trouveraient en phase d’extinction prolongée puisque leurs émissions de cris d’offrande sur la mangeoire habituelle ou de test ne sont suivies d’aucune réponse. Ceci pourrait expliquer que, bien qu’étant toujours maternelles, les poules émettent moins de cris d’offrande dans ce cas. Cette hypothèse est d’autant plus probable que divers auteurs comme Guyomarc’h ou Moffatt et Hogan ont mis en évidence de telles capacités d’apprentissage simple chez les poussins. L’hypothèse de l’existence de pro-
A.-M. Wauters, M.-A. Richard-Yris / C.R. Acad. Sci. Paris, Sciences de la vie / Life Sciences 324 (2001) 1021–1027
cessus complexes comme l’intentionnalité ne semble donc pas nécessaire pour interpréter les résultats obtenus dans notre étude. L’intervention d’une forme simple
de conditionnement permet une interprétation plus parcimonieuse des résultats obtenus.
1. Introduction
food calls they emitted [16]. Moreover, in the presence of their usual diet, hunger level positively affected food call production [16]. In addition, food calling in maternal hens is modulated by the caller’s social context: presence of chicks, behaviour of chicks and separation from chicks modified food call production [12, 27, 28]: for example, when food was present, hens uttered longer when chicks were in the same cage but did not have access to the food, than when they could approach the food and feed nearby [28]. Moreover, in the presence of food items, hens produced more food calls in the temporary absence of chicks than in their presence [16]. Similarly, when chicks were separated from their mother, who could still hear and see them, maternal hens uttered more food calls than when chicks were free in the same cage [28]. These data coincide with observations made under natural conditions by Stokes [6]. He observed that hens’ food calls became louder, faster and longer with increasing distance between hen and chicks as chicks mature. Therefore, in the presence of food, hens appeared to utter more food calls when their chicks were too far away and more generally when the chicks did not respond to their calls by going toward their mother’s head to eat. To explain the modulation of food call production, a straightforward hypothesis would be that hens could associate, by simple conditioning, their vocal production with the more or less rapid approach of chicks. This hypothesis implies that the repeated absence of approach and pecking of chicks following food calls induces a decline of the hen’s tendency to utter many food calls in the presence of palatable food items. In this study, we investigated whether the possibility for chicks to respond regularly to their mother’s calls could reinforce the hen’s tendency to utter many food calls when her chicks are temporarily absent. In other words, we investigated whether food calling is sensitive to ‘historical’ contextual conditioning with filial reinforcement [29].
Food associated calls have been reported in several primate species [1, for review] and in a number of bird species, including gallinaceous birds [2–7], common ravens [8], house sparrows [9] and cliff swallows [10]. Sound spectrograms reveal that the food calls of both domestic and red junglefowl chickens consist of a series of pulse-like sounds delivered at almost regular intervals [11–13]. These rhythmically repeated calls were generally uttered when a bird was frequently picking up and dropping either edible or inedible objects, that, usually, it did not swallow [4]. Descriptive studies indicate that food calls are usually produced by cockerels and broody hens with chicks, but are sometimes emitted by non broody hens [14–16] and more rarely by chicks [17]. Several studies reported that food calling cockerels attract hens to their vicinity [18] and food calling maternal hens attract chicks to the mother’s beak [12]. The study of Evans and Evans [19] supports the hypothesis of a functional reference for food calls, as signals with the property of functional reference should be sufficient, in the absence of eliciting stimuli and of other normally available cues, to permit receivers to select appropriate responses [25, 26]. The most detailed studies of food calls concern male chickens [20–24]. Male food calls appear to be induced by food items and by stimuli that predict reliably the availability of food [23]. Some studies also revealed that the rate at which males produce food calls reflects their preference for a given food stimulus, so that it is higher for living mealworms than for less preferred items like their regular rations [20]. Other experiments revealed a social dimension of male food calls: cockerels uttered significantly more food calls when a hen was confined in an adjacent cage than when they were alone [21, 23] or when another male was present [21]. Nevertheless these observations raised two problems. First, the almost absence of emission when another male is present can be explained differently in function of the type of information (simply ‘food’ or ‘food and propensity to share it’) carried by the signal. The second problem is that, during tests, each male was separated from his familiar female. The absence of a response from the receiver (the hen), more than its simple presence, could be at the origin of the higher food call rate. Furthermore, food calling is sensitive to contextual conditioning: food calling in the absence of a female increased after training in her presence and decreased again after training in her absence [15]. Maternal hens also modulate their production of food calls in relation to the quality of the food they have found: the more the maternal hens preferred a food type, the more
2. Material and methods 2.1. Subjects
Seventeen two-year-old domestic hens from a commercial meat-strain (‘Elevage Gauguet’) were housed in individual wire-mesh cages (100 × 70 × 60 cm) with opaque lateral partitions and nest-boxes. Thus, each bird was isolated visually but not auditorily from the others. Birds were maintained under a constant artificial photoperiod (14L:10D); temperature of the experimental room was 20 ± 2 °C. Apart from a short period of food restriction, all animals were provided with water and a mixture of whole wheat and commercial diet at libitum.
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2.2. Induction of maternal behaviour
To induce maternal behaviour, laying hens were deprived of food for 2 days and then were given only restricted rations (50 g·bird–1·day–1) of whole wheat for the following 6 days in order to stop egg laying and to ensure rapid onset of maternal responses [30]. This method, routinely used in our laboratory, may appear severe but no ill effects have even been recorded following this treatment (weight loss = 5 %). Thereafter, food was provided ad libitum. Maternal behaviour was experimentally induced 2 days after the end of the food-restriction period: the hens were shut in their nest-boxes at lights out, and 2 h later two newly hatched chicks were gently placed under each hen. The doors of the nest-boxes were removed the following morning, 30 min before the lights came on, to allow access to the entire cage. All hens giving chicks following this procedure accepted them and showed complete brooding behaviour with clucking and food calls. These chicks remained with their foster mother for 7 days and were then replaced by the newly hatched chicks used in experiment 1. When chicks were 8 days old, they were replaced by the newly hatched chicks used in experiment 2. 2.3. Test procedure
Two successive experiments (experiments 1 and 2) were conducted, using two types of food. As food palatability can influence food calling in maternal hens [16], experiments were first conducted with a highly preferred food item (experiment 1), and then, with the hens’ usual feed (experiment 2). For these experiments, the same hens were used with two different batches of chicks. During each experiment, broody hens were tested three times a day when their chicks were 3 and 4 days old. A test consisted in presenting a dish with food for 3 min in the hen’s home-cage. The tests were always carried out in the chicks’ absence. They started 1 h 30 after lights-on and were replicated 3 times during the day, at an interval of 3 h. The hens were tested in two different situations: – Situation A: the hens were with chicks all the time except during the tests. The chicks were removed, from their cage 2 min before each test and placed in a distant, heated room. They were returned to their mother’s cage after each 3-min test. – Situation B: the chicks were removed from their mother’s cage 30 min before the first test and were returned only 15 min after the last test of the day. To ensure that the hens were presented to the same experimenter-effect in the two situations, in the situation B the observer opened the cage and placed her hands in it as many times as she had to do it in situation A. Eight hens were tested in situation A when the chicks were 3 days old and in situation B the next day, when the chicks were 4 days old. The other nine hens were tested in the reverse order.
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Each test began when a transparent plastic dish (9 cm in diameter, 5 cm deep), fixed onto a small piece of wood, was introduced into the cage. In experiment 1, each hen was presented a highly preferred food item called ‘wormmash’ [16]: 5 mealworms on 50 g of wet mash (25 g of pellets and 25 g of water). In experiment 2, each hen was presented 50 g of a mixture of whole wheat and commercial ‘starter’ diet called ‘usual feed’. During the 3-min test the following measures were recorded: – The quantity of a hen’s feeding activity was estimated by the number of 15-s periods when it was observed. – The number of food calls for each 15-s period. Food calls were easily identified by ear and were counted directly as the observer heard them. At the same time, the vocalizations were tape-recorded and were blindly counted again after each observation. A microphone -LEM EMU4535-, connected to a tape-recorder -Marentz CP430-, was used to record vocalizations. Observations and vocalization recordings ended after 3 min. However, in all cases, after a test, the food dish was left in the cage for 3 more min. As the hens tested in situation A were reunited with their chicks at the end of each 3-min test, they had the possibility to see their chicks respond to their food calls by pecking in the dish, a reaction they otherwise experience all the time when they utter food calls at their usual feeding trough. The maintenance of the maternal state of hens was tested after the end of the last test of the day by recording their behaviour: a hen that clucked, food called and accepted the chicks under her when they were returned to their mother’s cage was considered to be maternal. 2.4. Statistical analyses
For each experiment, i.e., for each type of food presented, the data were analysed using a repeated-measures ANOVA with factors for test situation (A or B) and test number (1, 2 or 3), followed, if appropriate (P < 0.05), by further post hoc analysis using Student paired t-tests and Bonferroni–Dunn tests.
3. Results In situation B, as in situation A, all hens uttered clucks, food calls and accepted their young under them after the last test of the day, indicating that they were still maternal. Although maternal hens uttered significantly more food calls in the presence of their preferred food (worm-mash) than in the presence of their usual feed, in both cases the possibility to interact or not with chicks influenced the number of food calls uttered during tests (figure 1). Hens, in situation B, when chicks were removed all day, uttered significantly (P < 0.0001) fewer food calls after the first test than in situation A when chicks were returned to their mother immediately after each test. As in other experiments [16], we obtained a similar result when only the number of 15-s periods were considered (P < 0.008).
A.-M. Wauters, M.-A. Richard-Yris / C.R. Acad. Sci. Paris, Sciences de la vie / Life Sciences 324 (2001) 1021–1027
Table I. Pecking during tests.
percentage of 15-s periods
Test 1
during which hens pecked (Mean ± SE)
Test 2
Test 3
M
SE
M
SE
M
Se
Wet mash + mealworms brief separation (A) continuous separation (B)
92.2 95.6
4.3 3.4
96.6 91.2
2.4 3.8
90.7 84.8
3.7 5.7
Wheat / commercial ‘starter diet’ brief separation (A) continuous separation (B)
90.7 90.7
4.2 5.1
80.4 74.0
8.1 7.9
82.8 93.1
8.7 3.7
4. Discussion
Figure 1. Food Calling by Maternal Hens during Tests. In situation A , chicks were returned to their mother after each 3 min test; in situation B , hens remained alone all day. N: mean number of food calls emitted during a test. *: significant differences between situations for each test (Student paired t-test, n = 17, p < 0.05). a: significant differences (p < 0.05) between test 1 and other tests for each situation (Bonferroni–Dunn post hoc test, n = 17).
In the presence of their preferred food as well as in the presence of their usual feed, the hen’s capacity to utter food calls varied in relation to test number (Bonferroni–Dunn, P < 0.05) (table I, figure 1): the number of food calls decreased with time. On the other hand, pecking, estimated by the number of 15-s periods when hens pecked, did not vary significantly with test number (P > 0.05) (table I).
Data presented here confirm that maternal hens are able to utter food calls in the presence of food even in the absence of their chicks [12, 16, 28]. In addition, when a hen always remained with her chicks that were only removed during the short time each test lasted (situation A), she uttered significantly more food calls than when mother-chick separation lasted longer and began 30 min before the first test. In situation A, hens could interact freely with their chicks all day long. This constant presence alone could maintain a strong tendency in the hen to utter food calls during the tests. Similarly, Sherry [12] observed that hens presented with a mealworm produced food calls for longer just after they had been separated from their young than when they could see them. He suggested that this call may also be used by the hen to gather her brood. The underlying idea suggested by this author is that this call is used intentionally by hens to attract their chicks. However, this interpretation does not seem to be sustained by some other observations. Indeed, if this was a hard and fast rule, we could suppose that hens temporarily deprived of their chicks would also utter many food calls when food is absent or not very palatable. However, this does not seem to be the case because, when no food was present during a test, isolated hens uttered very few food calls or none at all [28]. Another interpretation can be done if we refer to the behaviour of chicks reared in natural conditions. When chicks can interact freely with their mother, they generally respond by approaching her rapidly and pecking each time the hen utters food calls [17]. No doubt hens are able to learn that their food calls are nearly always followed by the approach of their chicks. This associated approach and/or pecking by chicks could be a social reinforcement for the hens. When they have been deprived of their chicks for several hours, like in situation B, the hens would be in a state of prolonged extinction insofar as their food calls uttered when they were pecking in the feeding trough were not followed by any response. This could explain why, in this situation, hens, that were still maternal, uttered fewer food calls than in situation A. Several authors have shown that chickens possess similar simple learning capacities. Guyomarc’h [31] showed that chicks learned, through
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simple conditioning, the semantic value of the hen’s food call. Similarly, Moffatt and Hogan [32] showed that although 5-day-old chicks have a prefunctional tendency to respond more readily to faster than to slower rates of food calls, this tendency could be modified by experience. Evans and Marler [23] showed that food calling by cockerels is not limited to edible food items but that it is also associated with stimuli that have, in the past, reliably predicted the presence of food. In addition, maternal hens that had only seen their chicks during daytime (12 days ago) produced fewer food calls in a test when chicks were free, than other maternal hens [33]. The authors hypothesized that hens, that had only seen chicks, had never experienced complete approach responses following food calls during these 12 days because they were separated from chicks and this could explain why these hens subsequently emitted fewer food calls during a test. Each individual historical context would therefore be liable to modulate the quantity of food calls that a maternal hen is likely to utter in the presence of food. On the other hand, in the experiment described here the number of food calls uttered decreased with test number regardless of food type. It is as if replication of the same test conditions during the same day induced a reduction of the hen’s tendency to utter many food calls. A similar tendency was described by Sherry [12] concerning daily tests in the absence of chicks. Even though we have no definite explanation of this decline, we can suggest several hypoth-
eses. Under our experimental conditions, three tests were conducted during the same day and the hens had permanent access to food in their home cage. The decline in the number of food calls recorded could possibly be the result of a decline in interest for the food presented in relation to the animals’ hunger level, as their hunger necessarily decreased between test 1 and test 3. Hunger level is known to modulate the quantity of food calls uttered by cockerels [23] as well as by hens [16]. Nevertheless, it must be remembered that pecking, estimated by the number of 15-s periods when pecking in the dish was observed, did not vary significantly with test number. In addition, the effect of the time of day when the food test was presented must not be dismissed. This greater tendency to food call in the morning has also been reported in primates [34, 35] and could be due to fasting during the night, but also to ultradian feeding or arousal rhythms. Finally, food calling in most gallinaceous birds is known to be stimulated by uncommon food items [4, 6, 14, 16]. Replicate presentations during the same day of the same food type could induce a decline of its relative novelty which seems to stimulate the emission of a greater number of food calls.
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To conclude, the supposed existence of complex cognitive processuses, as intentionality, is not necessary to interpret the obtained results. These results rather form a possible role of the operant conditioning in the development of a naturaly occuring communication behaviour.
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