Charlène A. Ruppli

Individual vocal signatures in barn owl nestlings: does individual recognition have an adaptive role in sibling vocal competition?

To compete over limited parental resources, young animals communicate with their parents and siblings by producing honest vocal signals of need. Components of begging calls that are sensitive to food deprivation may honestly signal need, whereas other components may be associated with individual‐specific attributes that do not change with time such as identity, sex, absolute age and hierarchy. In a sib–sib communication system where barn owl (Tyto alba) nestlings vocally negotiate priority access to food resources, we show that calls have individual signatures that are used by nestlings to recognize which siblings are motivated to compete, even if most vocalization features vary with hunger level. Nestlings were more identifiable when food‐deprived than food‐satiated, suggesting that vocal identity is emphasized when the benefit of winning a vocal contest is higher. In broods where siblings interact iteratively, we speculate that individual‐specific signature permits siblings to verify that the most vocal individual in the absence of parents is the one that indeed perceived the food brought by parents. Individual recognition may also allow nestlings to associate identity with individual‐specific characteristics such as position in the within‐brood dominance hierarchy. Calls indeed revealed age hierarchy and to a lower extent sex and absolute age. Using a cross‐fostering experimental design, we show that most acoustic features were related to the nest of origin (but not the nest of rearing), suggesting a genetic or an early developmental effect on the ontogeny of vocal signatures. To conclude, our study suggests that sibling competition has promoted the evolution of vocal behaviours that signal not only hunger level but also intrinsic individual characteristics such as identity, family, sex and age.

Social rules govern vocal competition in the barn owl

To resolve the share of limited resources, animals often compete through exchange of signals about theirrelative motivation to compete. When two competitors are similarly motivated, the resolution of con-flicts may be achieved in the course of an interactive process. In barn owls, Tyto alba, in which siblingsvocally compete during the prolonged absence of parents over access to the next delivered food item, weinvestigated what governs the decision to leave or enter a contest, and at which level. Siblings alternatedperiods during which one of the two individuals vocalized more than the other. Individuals followedturn-taking rules to interrupt each other and momentarily dominate the vocal competition. These socialrules were weakly sensitive to hunger level and age hierarchy. Hence, the investment in a conflict isdetermined not only by need and resource-holding potential, but also by social interactions. The use ofturn-taking rules governing individual vocal investment has rarely been shown in a competitive context.We hypothesized that these rules would allow individuals to remain alert to one anothers motivationwhile maintaining the cost of vocalizing at the lowest level.© 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd.

Efficiency and Significance of Multiple Vocal Signals in Sibling Competition

Animals can compete for resources by displaying various acoustic signals that may differentially affect the outcome of competition. We propose the hypothesis that the most efficient signal to deter opponents should be the one that most honestly reveals motivation to compete. We tested this hypothesis in the barn owl (Tyto alba) in which nestlings produce more calls of longer duration than siblings to compete for priority access to the indivisible prey item their parents will deliver next. Because nestlings increase call rate to a larger extent than call duration when they become hungrier, call rate would signal more accurately hunger level. This leads us to propose three predictions. First, a high number of calls should be more efficient in deterring siblings to compete than long calls. Second, the rate at which an individual calls should be more sensitive to variation in the intensity of the sibling vocal competition than the duration of its calls. Third, call rate should influence competitors’ vocalization for a longer period of time than call duration. To test these three predictions we performed playback experiments by broadcasting to singleton nestlings calls of varying durations and at different rates. According to the first prediction, singleton nestlings became less vocal to a larger extent when we broadcasted more calls compared to longer calls. In line with the second prediction, nestlings reduced vocalization rate to a larger extent than call duration when we broadcasted more or longer calls. Finally, call rate had a longer influence on opponent’s vocal behavior than call duration. Young animals thus actively and differentially use multiple signaling components to compete with their siblings over parental resources.

Nestling barn owls assess short-term variation in the amount of vocally competing siblings

Assessing the amount of rivals is crucial to optimally adjust investment into a contest. If laboratory animals show numerical abilities, little is known about the ecological implications particularly in young animals. The two to nine barn owl (Tyto alba) siblings vocally compete for priority of access to food resources before parents actually deliver them. In dyads, the individual that vocalizes at the highest rate in the absence of parents deters its siblings from competing for next delivered prey. We tested the novel hypothesis that to optimally adjust vocal investment, barn owl nestlings assess how many of their siblings are currently competing. To singleton owlets, we broadcasted a fixed global number of calls emitted by one, two or four pre-recorded unfamiliar nestlings. We could thus distinguish the independent effect on singletons’ vocal behavior of the global number of calls produced by a brood from the number of competitors that produced these calls. Overall, nestlings retreated more from vocal contest when facing more competitors. However, in front of one highly motivated competitor, nestlings refrained from vocalizing to a larger extent than when competing against more but less motivated individuals. Therefore, young animals assess variation in the number of currently competing siblings based on individual-specific vocal cues.

Corticosterone Promotes Scramble Competition Over Sibling Negotiation in Barn Owl Nestlings (Tyto alba)

In species with parental care, siblings compete for access to food resources. Typically, they vocally signal their level of need to each other and to parents, and jostle for the position in the nest where parents deliver food. Although food shortage and social interactions are stressful, little is known about the effect of stress on the way siblings resolve the conflict over how food is shared among them. Because glucocorticoid hormones mediate physiological and behavioral responses to stressors, we tested whether corticosterone, the main glucocorticoid in birds, modulates physical and vocal signaling used by barn owl siblings (Tyto alba) to compete for food. Although corticosterone-implanted (cort-) nestlings and placebo-nestlings were similarly successful to monopolize food, they employed different behavioral strategies. Compared to placebo-nestlings, cort-individuals reduced the rate of vocally communicating with their siblings (but not with their parents) but were positioned closer to the nest-box entrance where parents predictably deliver food. Therefore, corticosterone induced nestlings to increase their effort in physical competition for the best nest position at the expense of investment in sib–sib communication without modifying vocal begging signals directed to parents. This suggests that in the barn owl stress alters nestlings’ behavior and corticosterone could mediate the trade-off between scramble competition and vocal sib–sib communication. We conclude that stressful environments may prevent the evolution of sib–sib communication as a way to resolve family conflicts peacefully.

Nocturnal, diurnal and bimodal patterns of locomotion, sibling interactions and sleep in nestling Barn Owls

AbstractTemporal variation in physical activity is mainly determined by the day–night cycle. While this may be true for diurnal species whose vision at night is often poor, the situation might be more complex in nocturnal animals as many such species can see both in the dark and in the daylight. We examined in Barn Owl (Tyto alba) nestlings whether temporal variation of behavioural activities and sleep is shaped by parental feeding visits occurring during the first part of the night and the extent to which they also occur during daylight hours. We measured several behaviours in 280 individuals from 90 broods recorded in 4 years. Parental feeding visits progressively declined in frequency from the beginning to the end of the night, and a number of offspring behaviours followed the same pattern of activity (feeding, vocalization and self-preening). Surprisingly, nestlings were awake not only at sunset, but also at sunrise. Several behaviours (locomotion, wing flapping and sibling interactions, such as pecking and allopreening among nestlings) showed peaks of activity at sunset and sunrise, suggesting that they were performed for other reasons than to interact with parents. Allopreening was performed more often during the day than at night. We conclude that although adult Barn Owls are nocturnal, nestlings display a complex temporal pattern of activity that is governed not only by feeding but also by other unknown factors.ZusammenfassungNächtliche, tägliche und bimodale Muster der Lokomotion, der Interaktionen mit Geschwistern und des Schlafs bei Schleiereulennestlingen Der zeitliche Verlauf der körperlichen Aktivität wird hauptsächlich vom Tag-Nacht-Rhythmus bestimmt. Besonders tagaktive Arten sind oft nicht in der Lage nachts zu sehen, während nachtaktive Arten sowohl am Tag als auch nachts sehen können. Wir untersuchten an Schleiereulennestlingen (Tyto alba), ob zeitliche Variation von Verhalten und Gehirnaktivität von den elterlichen Besuchen in der ersten Hälfte der Nacht abhängen und ob Aktivitäten während des Tages ausgeführt werden. Wir bestimmten Verhaltensweisen von 280 Individuen aus 90 Bruten über vier Jahre. Elterliche Fütterungsbesuche nahmen über die Nacht stetig in der Frequenz ab, und einige der Verhaltensweisen der Nestlinge folgten diesem Muster (Fressen, Rufen und Putzen). Erstaunlicherweise waren Nestlinge nicht nur bei Sonnenuntergang wach, sondern auch bei Sonnenaufgang. Einige Verhaltensweisen (Lokomotion, Flügel schlagen und Interaktionen mit Geschwistern wie Picken und gegenseitiges Putzen) zeigten hohe Aktivität bei Sonnenuntergang und –aufgang, was darauf hindeutet, dass sie aus anderen Gründen ausgeführt wurden als mit den Eltern zu interagieren. Gegenseitiges Putzen wurde tagsüber öfter durchgeführt als nachts. Zusammenfassend ist zu sagen, dass Schleiereulen zwar nachtaktiv sind, Nestlinge aber ein komplexes Aktivitätsmuster zeigen, das durch die elterliche Fütterung vorgegeben ist, aber auch durch weitere, noch unbekannte Faktoren bestimmt ist.

Responsiveness to siblings’ need increases with age in vocally negotiating barn owl nestlings

In animal societies, individuals should optimize the way they behave in relation to the behavior displayed by their conspecifics. This social competence, i.e., the ability to adjust behavior to the social context, can vary between individuals, but also improve with age and experience. This aspect, although important, has rarely been studied. We tested whether the ability to adjust behavior to siblings develops with age in barn owl nestlings (Tyto alba). In this species, young siblings show intense social interactions referred to as “sibling negotiation.” Indeed, because parents bring a single indivisible food item at each visit to the nest, all the effort invested in sibling competition is only paid back in the nestling that is able to monopolize the food item. Therefore, before the arrival of parents, siblings vocally inform each other about their relative hunger level so that they can optimally invest in sibling competition, with the most vocal, and hence hungry, nestling momentarily deterring its siblings from competing. This process implies that siblings have the ability to adjust their behavior in relation to the behavior of their siblings, a process that could change with age. In a series of experiments, we examined how nestlings of different ages respond to the vocal behavior of siblings. We show here that older nestlings adjusted their vocal behavior more finely than younger nestlings in relation to the behavior of their siblings. Elders also more readily refrained from eating in front of a hungry sibling. These patterns could arise because owlets’ social competence develops with age or because they adopt different competitive and cooperative strategies according to their age.Significance statementIn sibling barn owls, competition for food brought by parents is settled by vocalization. Highly vocal owlets induce their siblings to call less and to let them eat in priority once parents are back with a prey item, a process referred to as “sibling negotiation.” Nestling barn owls adjust their investment in sibling competition according to two parameters: their hunger level and the vocal behavior of their siblings. We analyzed the relative importance of these two parameters in differently aged owlets. Younger owlets adjusted the intensity of vocalizing primarily in relation to their own hunger level, which was efficient in modifying older nestlings’ behavior, as older nestlings readily withdrew from vocal contest and refrained from eating in front of highly vocal siblings. Hence, social adjustment changed with age in owlets, older ones being more sensitive to the signals of need of their siblings.