Responsiveness to siblings' need increases with age

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Jun 22, 2017 - social contacts behave more appropriately in the contexts of dominance interactions and brood care, compared to single- mother reared mice ...
Behav Ecol Sociobiol (2017) 71:109 DOI 10.1007/s00265-017-2342-0

ORIGINAL ARTICLE

Responsiveness to siblings’ need increases with age in vocally negotiating barn owl nestlings Amélie N. Dreiss 1 & Charlène A. Ruppli 1 & Alice Delarbre 1 & Christof Faller 2 & Alexandre Roulin 1

Received: 9 March 2017 / Revised: 22 June 2017 / Accepted: 23 June 2017 # Springer-Verlag GmbH Germany 2017

Abstract 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 Bsibling 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

Communicated by M. Leonard * Amélie N. Dreiss [email protected] Charlène A. Ruppli [email protected] Alice Delarbre [email protected] Christof Faller [email protected] Alexandre Roulin [email protected] 1

2

Department of Ecology and Evolution, University of Lausanne, CH-1015 Lausanne, Switzerland Audiovisual Communications Laboratory, Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland

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 statement In 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 Bsibling 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. Keywords Age . Communication . Competition . Cooperation . Sibling negotiation . Social competence . Social information

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Introduction Animals modulate their behavior in relation to biotic and abiotic components of their environment. When in conflict over limited resources, some animals can adjust their investment in competition according to the presence of an audience (Munn 1986) or the motivation and resource holding potential of opponents (Godfray 1995; Oliveira et al. 1998). An adjustment could avoid engaging in costly social interactions and help optimize the signal efficiency according to the likelihood of winning a contest (Dall et al. 2005; Arnott and Elwood 2008). In any conflict of interest, animals would benefit from communicating with conspecifics at the lowest level necessary to obtain the contested resource, hence minimizing the cost/benefit ratio of communication (Johnstone 1997). Instead of producing their signals of motivation and of competitive ability at a fixed level (Parker 1974; Maynard Smith 1982), some animals would tactically adjust their behavior to one another, step by step (Patricelli et al. 2011). The ability to adjust behavior to the social context can provide substantial fitness advantages for instance by reducing aggression from conspecifics (van Leeuwen et al. 2014), and enhancing survival success (Fischer et al. 2015) and mating behavior (Patricelli et al. 2002). However, this fine-tuning is potentially cognitively demanding as multiple rivals have to mutually perceive and compare their level of motivation and resource holding potential, and accordingly adjust their signaling level from moment to moment. In fact, the propensity to adjust to social factors can be related to several factors, including the cognitive ability to detect and process social signals (Taborsky and Oliveira 2012) or the cost of relying to social information relative to own motivation level (Giraldeau et al. 2002; Mesterton-Gibbons and Heap 2014). It is likely that this social responsiveness varies during the learning/development phase before adulthood, either because the cognitive social ability grows or because the need and competitive ability fluctuate. However, the emergence and the role of social responsiveness in young animals are poorly known. In some species, Bsocial competence,^ referring to the ability to adjust behavior to the social context (Taborsky and Oliveira 2012), develops during the early phases of life, rich social environments experienced during development promoting social competence (White et al. 2010; Fischer et al. 2015). For instance, communally reared mice exposed to frequent social contacts behave more appropriately in the contexts of dominance interactions and brood care, compared to singlemother reared mice (D'Andrea et al. 2007). Social interactions are essential in some altricial young, as they partly determine food share, sustained injuries, and ultimately survival and growth of young (Drummond 2006; Royle et al. 2012). The ability to adjust behavior to social interactions is present in some altricial young (Roulin 2002b; Marques et al. 2011), but whether this ability increases with age during development is less well investigated.

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Interaction between altricial siblings is not the only way social complexity can emerge (Scheiber et al. 2017). However, competition between altricial siblings is ideal to study the emergence of social competence at very early stages, because of the repeated social interactions between siblings taking place during the rearing period. In the barn owl, young siblings aged 3 weeks to 2 months not only beg for food from parents but also communicate vocally among each other throughout the night while parents are foraging. This sib-sib communication system enables siblings to resolve conflicts non-aggressively over priority of access to the next prey item delivered by a parent, a process referred to as sibling negotiation (Roulin 2002b). Because only one chick is fed per parental feeding visit, siblings are selected to optimally invest in competitive behavior according to the probability of monopolizing the next delivered prey item (Johnstone and Roulin 2003). When facing a highly vocal sibling, owlets withdraw from the vocal negotiation with their siblings and from begging at parent arrival (Roulin 2002b). Contrary to systems of cooperative begging (Johnstone 2004), such as in banded mongooses Mungos mungo (Bell 2007), barn owl nestlings do not benefit from the vocalization of nestmates to increase parental feeding (Roulin 2002b). Sibling negotiation has been studied in a few animal species (black-headed gulls (Mathevon and Charrier 2004), spotless starlings (Bulmer et al. 2008), meerkats (Madden et al. 2009), barn swallows (Romano et al. 2013)) and involves iterative behavioral adjustments between siblings (Dreiss et al. 2015b). This system is therefore ideal to study how animals finely adjust their social behavior to one another, a question that concerns many situations in the animal kingdom, beyond the social context of sibling negotiation. The adjustment of barn owl nestlings’ vocalization in the absence of parents is a balance between their own motivation and the competitiveness displayed by siblings. Owlets invest more effort in vocal signaling, in terms of number of calls and call duration, when they are hungry (Ruppli et al. 2013a), but withdraw from vocal contests when their siblings are highly vocal, i.e., when they globally emit many long calls (Roulin 2002b; Ruppli et al. 2013a), although they challenge one another by copying their call duration (Roulin et al. 2009; Dreiss et al. 2015b). Owlets also adjust their vocal behavior according to brood size and to the amount of vocalizing siblings (Roulin et al. 2000; Roulin 2002b; Ruppli et al. 2013b) or after having eavesdropped a vocal interaction (Dreiss et al. 2013b, 2015a). Additionally, owlets delay the timing of consumption of the food stored in the nest when they hear a hungry nestmate compared to when hearing a satiated one (Dreiss et al. 2016). Younger siblings are known to produce more and longer calls than their elder siblings (Dreiss et al. 2010b, 2014), but how differently aged nestlings react to negotiation is poorly known. In the present study, we investigated how differently aged owlets adjust their vocal investment and their feeding

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behavior both to intrinsic motivation (i.e., hunger level) and extrinsic social environment. To do so, we reanalyzed six previously published experiments performed between 2008 and 2013 on owlets aged between 20 and 45 days, in which we had not considered the way nestlings respond to the various experimental treatments according to their age. The present study allows us to test whether behavior adjustments vary with age in response to (1) own hunger level; (2) nestmate vocal investment, in particular, number of calls and call duration; (3) the number of vocal nestmates; and (4) eavesdropped vocalizations. According to previous studies, both number of calls and call duration reflect hunger level and high numbers of long calls induce nestmates to withdraw from vocal competition. We expect that the ability to respond to siblings’ social signals would improve with age, and hence, older individuals would better adjust investment in sibling negotiation in relation to the social context than younger individuals. Broods were taken to the laboratory at similar stages (when the eldest was 35–46 days), and age effect could reflect the absolute age or the rank in the hierarchy due to asynchronous hatching. We will hence discuss whether the age difference is due to experience, learning, need, competitive ability, and how to disentangle between the explanatory alternatives.

Methods Study population The studies were performed in western Switzerland (46° 4′ N, 6° 5′ E) on a population of wild barn owls breeding in nest boxes located in barns. This nocturnal species is monogamous with low rates of extra pair paternity (2%; Henry et al. 2013; Ducret et al. 2016). Eggs are laid on average every 2.5 days, from the end of February to mid-August. Females lay 1 to 12 eggs and start to incubate the clutch after the first egg has been laid. This behavior generates a pronounced within-brood age hierarchy among siblings. Parents hunt small mammals at night to feed their one to nine offspring (Roulin 2004a). Once offspring are thermo-independent at 2 to 3 weeks of age, the mother begins to hunt to provision the brood. We carried out the experiments after this age, when parents were naturally sleeping outside their nest box in another barn, and before nestlings take their first flight at around 55 days. Offspring eat by swallowing entirely the prey item or cutting it into pieces before consumption. Experimental and statistical procedures We examined the vocal and behavioral responses of nestlings in interaction with age (as a continuous covariate) during six experiments performed between 2008 and 2013, on owlets brought temporarily to the laboratory. We performed similar

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statistical analyses as published in previous papers (Dreiss et al. 2013b, 2016; Ruppli et al. 2013b, a), except that we added the interaction between owlet age and the experimental or studied effects. To draw figures and interpret the effect, when this interaction was significant, we performed additional analyses using age as a two-level categorical variable, with the median age (which varied according to experiments from 33 to 36 days) as the cutoff point. We did not test additional effects that were not found in previous studies, and we chose to use the same parameters as the previous published studies. To be consistent with previous published analyses, in studies 1, 3, 4, and 5, the number of calls and call duration were used as the response variables. In study 2, we analyzed only call duration, because nestlings copy the call duration of their nestmate in the short term when they interact. In study 5, we analyzed the calling latency (i.e., the time elapsed after the emission of a nestmate call), like in the published study, because latency was the parameter manipulated in the playback treatment. Moreover, we aimed at examining the immediate response to single calls. The conclusions published in previous studies still hold, and we focus our discussion on the differential behavioral responses due to age. Nestling age was estimated shortly after hatching by measuring the length of the left flattened wing from a bird’s wrist to the tip of the longest primary (Roulin 2004b). We briefly describe the essential information about the six experiments. Vocal and feeding behaviors were recorded and analyzed blindly to treatment and individual age and identity. Complete methods and ethical notes can be found in previous papers. All statistical analyses were performed with the software SAS v.9.3 (SAS Institute Inc., Cary, NC, USA). Means are given ± standard error. Assumptions for the models used were verified in each test (homoscedastic and normal distributions of variables and residuals for linear mixed models; overdispersion of generalized mixed model, with departure of the scaled Pearson statistic from 1). The complete models without selection are presented in the tables in the BResults^ section. Vocal adjustment to hunger level (Ruppli et al. 2013a) Hungry nestlings produce more calls and longer calls than satiated ones, as demonstrated when manipulating food supply in pairs of siblings (68 females and 76 males, 35 ± 1 day old, range 22–46) from 41 broods in 2008. We used the same experience to determine whether this adjustment was related to age. After one night of acclimation, we recorded the calls of sibling pairs from 21:00 until 23:40 on the second and third nights in the laboratory. On one of the two nights, chosen randomly, we food-deprived the two individuals (no food given during the preceding 28 h) or food-satiated them (from midnight to 16:00 on the recording day, we offered 130 g of laboratory mice, which exceeds their daily food requirement).

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Mean call duration and total number of calls over the recording session were analyzed with linear mixed model and generalized mixed model for overdispersed data (Joe and Zhu 2005), respectively, with individual identity nested in both sibling pair and brood identity as random factor. Food treatment and sex were included as fixed factors and age as a covariate.

Mean call duration and number of calls per playback sequence were analyzed with linear mixed model and generalized mixed model (Poisson distribution), respectively, with individual nested in brood identity as random factor. The call duration and the call rate of the playback nestmate were included as fixed factors. Sex and the order of playback sequence were additional fixed factors and age was a covariate.

Vocal adjustment to sibling vocalization—two-chick broods (Dreiss et al. 2015b)

Vocal adjustment to the number of nestmates—playback experiment (Ruppli et al. 2013b)

When siblings exchange calls interactively, they produce calls of similar duration as their sibling (Roulin et al. 2009; Dreiss et al. 2015a). We used the experiment performed in 2008 to determine whether this tendency to copy the call duration of siblings was related to age. We considered food-deprived pairs, as they exchange more calls than food-satiated ones (Dreiss et al. 2015a). We analyzed whether the duration of a call produced after a vocal interruption by a sibling was correlated with the duration of the sibling call in interaction with age. Call duration of focal individual was set as dependent variable in a linear mixed model, with individual identity nested in both sibling pair and brood identity as random factor. Because the influence of the call of a sibling is likely to fade with time, we only considered the calls produced at short-term intervals, i.e., if the pause between two successive owlet calls was 36 days] 0.56 ± 0.12, P < 0.0001; estimate for call duration in young nestlings 0.10 ± 0.01 s, P < 0.0001, and in older nestlings 0.06 ± 0.01 s, P < 0.0001).

Experiment 2. Vocal adjustment to sibling vocalization—two-chick broods Nestlings adjusted their call duration to one another differently with age (Table 2; interaction age × duration of previous sibling’s call). Older nestlings appeared to copy the call duration of their nestmate to a higher extent than younger ones (estimate for call duration in young nestlings [≤36 days] 0.04 ± 0.01 s, P < 0.0001, and in older nestlings [>36 days] 0.15 ± 0.01 s, P < 0.0001; Fig. 2).

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Table 1 Vocal adjustment to hunger according to age in nestling barn owls

Total number of calls (df = 142)

Food treatment (deprived vs. satiated) Age Sex (female vs. male) Age × food treatment

Mean call duration (s) (df = 94)

Estimate ± SE 2.77 ± 0.81

F 11.66

P 0.001

Estimate ± SE 0.22 ± 0.06

F 12.44

P 0.001

0.05 ± 0.02 −0.11 ± 0.17 −0.05 ± 0.02

1.56 0.38 5.72

0.21 0.54 0.018

−0.001 ± 0.002 0.008 ± 0.024 −0.004 ± 0.002

4.88 0.10 4.98

0.030 0.75 0.028

Generalized mixed model (for total number of calls) and linear mixed model (for mean call duration), for 144 nestling barn owls recorded in pairs in 2008. Age was used as continuous variable

Experiment 3. Vocal adjustment to nestmate vocalization—playback experiment

Experiment 4. Vocal adjustment to the number of nestmates—playback experiment

Owlets modified their number of calls in response to playback call rate differently with age (Table 3; interaction with age). Older nestlings decreased their number of calls to a higher extent in response to increased playback call rate (Fig. 3a; estimate for number of calls [2 vs. 10 playback calls/min] in young nestlings [