Turn-taking is maintained in multi-participant groups of more than three individuals

Coordination is a fundamental aspect of social living, underlying processes ranging from the maintenance of group cohesion to the avoidance of competition. Coordination can manifest as synchronization, where individuals perform the same action at the same time but can also take the form of anti-synchronization or turn-taking. Turn-taking has mainly been studied in the context of the development of language [] due to the fact that it is a universal feature in all languages and has been found to appear early in infancy []. Recently, turn-taking has received attention in animal communication research [] as a potential foundation on which social communication was formed []. In this study, we describe turn-taking in group-wide vocal interactions of meerkats (Suricata suricatta) during low-conflict sunning behavior, which is accompanied by the production of specific “sunning calls.” We show that sunning-call production is socially stimulated and that at the group level, meerkats avoid overlap, thus fulfilling a key principle of turn-taking []. Through observational data and playback experiments, we show that these group-level patterns arise from two individual-level rules: call inhibition over short timescales, which prevents mutual interference, and call excitation over longer timescales, which stimulates further group calling. These simple rules suggest that hierarchy formation and turn allocation are not required for achieving group-wide coordination of communication. We also suggest that the potential bonding function of turn-taking shown in humans might have similar effects in animal interactions.

Social coordination in animal vocal interactions. Is there any evidence of turn-taking? The starling as an animal model.

Although our analysis of natural sunning interactions suggests that short-term inhibition and long-term social stimulation underlie the observed calling dynamics, observational data alone cannot demonstrate a causal relationship between the calls of conspecifics and the call timing of focals. Moreover, vocal behavior can often be affected by conspecific signals and cues in non-acoustic modalities, as well as by environmental events. To experimentally test our proposed mechanism of overlap avoidance, we performed a series of playback experiments. Sunning calls were played back to focal meerkats standing at least 1 m away from a closest neighbor, thus making the played-back calls the closest and potentially strongest acoustic effector of focal calling behavior. We assessed the timing of calls from the focal individual with respect to the timing of calls from the playback stimulus. As a control, the same individuals were also recorded in the absence of a playback stimulus, and the timing of their calls was assessed relative to the same time points in which playback calls occurred in the experimental condition. In agreement with the patterns seen in natural sunning data, results from these playbacks also showed consistency with the inhibition hypothesis ( Figure 3 B). Moreover, playback results confirmed the same timescale-dependent pattern as seen in natural observations, with focal individuals reducing their call rates relative to the control over short time windows after a playback call and increasing them over long timescales ( Figure 4 B). The results of this manipulation demonstrate a causal relationship between conspecific calls and the focal call timing. This also confirms that turn-taking in meerkats can be efficiently driven by audible signals only and is not a byproduct of unobserved factors such as visual or olfactory cues.

The finding that an individual’s calls are inhibited by the calls of others could be seen as contradictory to the result that calls are socially stimulated; however, these effects could in fact coexist if they operate over different timescales. To investigate this idea, we measured the focal individual’s call rate over a range of different time windows immediately following each background call or at random times as a control. Meerkats showed a timescale-dependent pattern of call rate following conspecific calls. Over short timescales (<0.2 s) following a background call, a focal’s call rate fell below the control rate, indicating a local inhibition by the incoming vocal signals. However, over longer timescales after a background call, the focal call rate increased beyond the control baseline in agreement with the results of a positive social stimulation ( Figure 4 A).

In both cases, focal individual call rate is suppressed 0–∼0.2 s after a call relative to the control and enhanced over longer time windows. Shaded areas denote 95% confidence intervals generated by block bootstrapping

(B) Mean focal individual call rate computed over increasing lengths of time windows immediately following a playback call (circles) or at the equivalent time in the control condition (triangles).

(A) Mean focal individual call rate (percentage of time occupied by vocal signals; y axis) during natural vocal interactions computed over increasing lengths of time windows (x axis) immediately following a conspecific call (circles) or at randomly positioned start times (triangles).

Individual Call Rate Is Suppressed Immediately after a Conspecific’s Call but Enhanced over a Longer Timescale in Both Natural Observations and Playback Experiments

Figure 4 Individual Call Rate Is Suppressed Immediately after a Conspecific’s Call but Enhanced over a Longer Timescale in Both Natural Observations and Playback Experiments

To tease apart the individual-level mechanisms giving rise to overlap avoidance at the group level, we examined in detail the timing of calls given by focal and background individuals. Following Takahashi et al. [], we first tested whether the pattern of overlap avoidance seen in meerkats is consistent with one of two simple mechanisms. According to the reset hypothesis, individuals have a typical distribution of intervals between calls, and hearing the call of another individual resets the clock on this interval distribution. If this hypothesis is true, the distribution of intervals between consecutive focal calls should be the same as the distribution of intervals between a background call and a focal call heard consecutively. According to the inhibition hypothesis, a call heard from another individual inhibits a focal individual’s call but does not affect subsequent calling behavior. Thus, the distribution of intervals between two focal calls should be the same as the distribution of those in a randomized dataset in which focal call tracks are paired randomly with background call tracks drawn from our dataset, with overlapping calls removed to simulate inhibition. We tested the support for both of these hypotheses in meerkat sunning interactions (see STAR Methods ). The results show that our data are broadly consistent with the inhibition hypothesis ( Figure 3 A, compare blue and green lines) and inconsistent with the reset hypothesis ( Figure 3 A, compare gray and green lines; KS test: D = 0.502, p < 0.001), supporting the idea that overlap avoidance is driven by meerkats locally inhibiting their calls when they hear others calling. Furthermore, in contrast to what has been found in dyadic interactions in marmosets and humans [], calling behavior of meerkats did not appear to be periodic ( Figure S3 C), suggesting that more complex mechanisms such as phase locking and entrainment are unlikely to be at play.

(A and B) Observed inter-bout interval distributions of sunning calls (green) are consistent with expected distributions for the inhibition hypothesis (blue), but not for the reset hypothesis (gray), in both natural observations (A) and playback experiments (B). Shaded areas represent 95% confidence intervals generated either by 100 different permutations of the background tracks used (in the case of inhibition hypothesis in A or from bootstrapping the interval data used to generate the distribution (1,000 draws with replacement).

Observed Inter-bout Interval Distributions of Sunning Calls Are Consistent with Expected Distributions for the Inhibition Hypothesis

Figure 3 Observed Inter-bout Interval Distributions of Sunning Calls Are Consistent with Expected Distributions for the Inhibition Hypothesis

To assess whether a turn-taking pattern exists in meerkat group sunning-call sessions, we analyzed individual recordings of 41 meerkats from 8 different social groups (a total of 23,180 calls). In the recordings, both the “focal” individual being recorded and other “background” meerkats nearby could be heard ( Figure 1 A). Focal calls were clearly distinguishable from sunning calls in the background. For each recording, we calculated the group-wide call rate (number of calls per sec) and the overlap rate. Overlap rate was calculated by summing the total amount of overlap time between focal-individual sunning calls and background sunning calls and then dividing this number by the maximum possible focal/background overlap time (i.e., the total amount of time vocalizing for either the focal or the background callers—whichever had the smaller total). This yielded a value between 0 and 1, with lower values of the overlap representing less overlap and thus more turn-taking ( Figure S4 A). Natural overlap rate was well below randomized null overlap rates generated by pairing each focal track with a random background track from a different day ( Figure 1 B; p < 0.01). This indicates that during group calling sessions, individuals avoid overlapping with conspecific signals, resulting in a turn-taking call pattern. Moreover, our data suggest that the temporal organization of meerkat calls is finely tuned to a pattern of overlap avoidance. We computed the overlap rate for “time-shifted” data in which the background calls WERE shifted by a fixed time interval relative to the focal calls for a given recording. The overlap rate was minimized at a time shift of 0 (i.e., natural calling data) and substantially increased even for small time shifts ( Figure 2 ). Additionally, the number of individuals that had a likely visual contact within a 2-m radius of the focal (median = 3, range = 1, 12), the total number of visible individuals (median = 7, range = 1, 23), and the group-wide call rate (median = 0.05 call/s, range = 0.009, 0.17) showed no effect on the overlap rate ( Table S4 ). These findings suggest that overlap avoidance is a robust phenomenon that is maintained in multi-participant vocal interactions as indicated by its insensitivity to more than 3-fold increase in both median group size and group call intensity. A general overview of the focal inter-call interval as a function of visible group size also did not show any relationship ( Figure S3 B).

(A and B) Overlap rate of natural sunning calls as a function of the time shift between focal and background calls on the level of single notes (A) and bouts (B). A time shift of 0 s is indicated by the dashed line and steeply increases with small time shifts.

(B and C) Overlap rate of natural sunning calls is significantly smaller than overlap rates for a randomized null model in which background tracks are permuted across recordings both on the level of single notes (B) and on the level of bouts (C). The gray bars show a histogram of the distribution of overlap scores calculated from 100 different permutations (y axis represents probability of a given overlap score in this null model). The dashed line shows the overlap rate of the observed data.

While sunning, meerkats frequently produced “sunning calls” ( Figure S2 ). These vocalizations were almost exclusively produced while sunning (92%) and very seldom while engaging in other activities (e.g., moving, grooming, foraging) during the sunning period ( Table S2 ). Calling behavior during sunning was strongly associated with the presence of other group members. Only in 7.7% out of 39 group scans (5-min intervals throughout each observation []) in which only one individual was out sunning did a focal subject produce sunning calls, whereas when others were present (340 group scans), individual sunning-call probability was significantly higher at 35.7% (binomial test: p < 0.0001). Adult (>1 year) individuals were more likely to produce sunning calls than juveniles (3–6 months) and pups (>3 months) (GLMM: F = 1.216, p < 0.001), whereas the dominance and sex of a focal individual had no significant effect on its probability of emitting sunning calls. When other group members were present, the probability of a meerkat emitting sunning calls depended on the proportion of them calling (GLMM: F = 388.854, p < 0.001; Figure S3 and Table S3 ), suggesting that calls are socially stimulated. Additionally, when the dominant female was vocalizing, individuals were less likely to call (GLMM: F = 65.011, p < 0.001; Table S3 B).

The majority of research on turn-taking in animals and humans has focused on dyadic, or in some cases triadic [], interactions. However, as vocal interactions in nature often occur in multi-participant settings, it remains unclear to what extent turn-taking patterns can persist in larger groups [] and what mechanisms underlie such coordination. Multi-participant turn-taking might rely on pre-set order, creating a rigid participation framework. An alternative mechanism is opportunistic turn usurping, which allows a free reshuffling of participation roles while maintaining the fundamental turn-taking []. Examining the mechanism of turn-taking in animal groups will allow us to determine whether the maintenance of multi-participant turn-taking can be a result of a spontaneous and cognitively simple process of self-assembly. To address this, we examined call dynamics in intra-group interactions among free-ranging meerkats, a social mongoose species [] with a complex vocal communication system []. Since calls produced in non-competitive interactions are more likely to show a turn-taking pattern than those produced in conflict situations [], we investigated the temporal organization of meerkat calls during low-conflict “sunning” behavior. During our data collection period, meerkats spent on average 44 ± 2 min (n = 91) sunning (sitting or standing on hind legs facing the sun with the ventral side of the body after emerging from their sleeping burrow). The time spent sunning was negatively correlated with minimum overnight temperature (generalized linear mixed model [GLMM]: F = 18.944, n = 97, p < 0.0001; Figure S1 and Table S1 ).

Discussion

Our results demonstrate a robust pattern of turn-taking in meerkat vocal interactions in the context of sunning sessions. Group calling sessions are characterized by a below-chance rate of call overlap indicative of turn-taking, which is maintained over a range of interaction intensities (call rates). Although we could not control for the number of vocalizing individuals in the recorded interactions, overall background call rate and the number of individuals present are a good proxy for interaction intensity. These variables showed no effect on the overlap rate despite being dispersed on a ∼20-fold range ( Table S4 ), and thus, turn-taking coordination was retained even at high call densities likely representing more than three active participants.

By considering the detailed individual-level calling dynamics, we show that the calls of other individuals both inhibit and stimulate individuals to call. These effects operate over different timescales, with call inhibition (i.e., a lower call rate per individual) immediately after the calls of others and call stimulation (i.e., a higher call rate per individual) over longer timescales. This multi-scale mechanism allows prolongation of group calling sessions while simultaneously facilitating avoidance of overlap among callers.

5 Takahashi D.Y.

Narayanan D.Z.

Ghazanfar A.A. Coupled oscillator dynamics of vocal turn-taking in monkeys. 1 Levinson S.C. Turn-taking in Human Communication--Origins and Implications for Language Processing. 18 Fröhlich M.

Kuchenbuch P.

Müller G.

Fruth B.

Furuichi T.

Wittig R.M.

Pika S. Unpeeling the layers of language: Bonobos and chimpanzees engage in cooperative turn-taking sequences. 19 Jones D.L.

Jones R.L.

Ratnam R. Calling dynamics and call synchronization in a local group of unison bout callers. 18 Fröhlich M.

Kuchenbuch P.

Müller G.

Fruth B.

Furuichi T.

Wittig R.M.

Pika S. Unpeeling the layers of language: Bonobos and chimpanzees engage in cooperative turn-taking sequences. 20 Greenfield M.D. Cooperation and conflict in the evolution of signal interactions. 6 Henry L.

Craig A.

Lemasson A.

Hausberger M. Social coordination in animal vocal interactions. Is there any evidence of turn-taking? The starling as an animal model. 21 Naguib M.

Kipper S. Effects of different levels of song overlapping on singing behaviour in male territorial nightingales (Luscinia megarhynchos). 22 Maltz D.N.

Borker R.A. A cultural approach to male–female miscommunication. 23 Rauber R.

Manser M.B. Discrete call types referring to predation risk enhance the efficiency of the meerkat sentinel system. 24 Manser M.B. Response of foraging group members to sentinel calls in suricates, Suricata suricatta. Individuals typically need to process incoming signals before emitting a response []. Typical response time for human conversation is 200 ms [], and a matching temporal relation between gestural exchange turns was recently found in bonobos (Pan paniscus) and chimpanzees (P. troglodytes) []. Additionally, simultaneous transmission and reception of signals of the same modality can create jamming [], impeding information transfer. Avoiding these two communicational problems may therefore require coordination among communicating parties. Similar to other types of coordinated display, turn-taking has been suggested to be a fundamentally cooperative behavior indicating shared interest among signalers for an effective exchange of information [], although see []. Violations of turn-taking rules are often negatively perceived, as they can indicate lack of attention, lack of experience [], or aggression []. Although the specific function and the informational content of meerkat sunning calls remain unclear, their apparent non-competitive context and the turn-taking pattern uncovered here suggest that they are a cooperative signal. Potentially, these calls might have a calming effect (as has been shown for acoustically similar sentinel calls []) and may play a role in maintaining group bond.

1 Levinson S.C. Turn-taking in Human Communication--Origins and Implications for Language Processing. 25 Barthel M.

Meyer A.S.

Levinson S.C. Next Speakers Plan Their Turn Early and Speak after Turn-Final “Go-Signals”. 26 McFarland D.H. Respiratory markers of conversational interaction. 27 Riest C.

Jorschick A.B.

de Ruiter J.P. Anticipation in turn-taking: mechanisms and information sources. 28 Torreira F.

Bögels S.

Levinson S.C. Breathing for answering: the time course of response planning in conversation. 1 Levinson S.C. Turn-taking in Human Communication--Origins and Implications for Language Processing. 18 Fröhlich M.

Kuchenbuch P.

Müller G.

Fruth B.

Furuichi T.

Wittig R.M.

Pika S. Unpeeling the layers of language: Bonobos and chimpanzees engage in cooperative turn-taking sequences. Early models developed to explain turn-taking in human conversation suggested that speaker transition is regulated by attending to turn termination cues produced by the current speaker []. More recent models add that signaler transition is achieved by an early turn planning before the occurrence of turn termination cues []. Parallels for these two principles can potentially be found in animal communication. Early turn planning in human conversation is indicative of the intention to communicate and stimulated by the incoming signals []. It is possibly parallel to the increase in signaling motivation stimulated by conspecific calls as demonstrated here by an overall increase in the probability to call when others do so. The use of turn termination cues and avoidance of overlapping talk in humans is similar to the observed transient call suppression possibly until a silent gap is perceived as a cue for the end of a turn. Another potential parallel between human and animal turn-taking organization is the similarity in the response time of approximately 200 ms found in humans [] and apes [], which also approximates the suppression time we find here in meerkats ( Figures 2 and 3 ).

9 Brush J.S.

Narins P.M. Chorus dynamics of a neotropical amphibian assemblage: comparison of computer-simulation and natural behavior. 11 Aihara I.

Mizumoto T.

Otsuka T.

Awano H.

Nagira K.

Okuno H.G.

Aihara K. Spatio-temporal dynamics in collective frog choruses examined by mathematical modeling and field observations. 10 Santner-Wolfartsberger A. Parties, persons, and one-at-a-time: conversation analysis and ELF. 10 Santner-Wolfartsberger A. Parties, persons, and one-at-a-time: conversation analysis and ELF. 29 Schegloff E.A.

Koshik I.

Jacoby S.

Olsher D. Conversation analysis and applied linguistics. 8 Sacks H.

Schegloff E.A.

Jefferson G. A simplest systematics for the organization of turn-taking for conversation. 30 Schegloff E.A. Parties and Talking Together: Two Ways in Which Numbers Are Significant for Talk-in-Interaction. 31 Greenfield M.D.

Tourtellot M.K.

Snedden W.A. Precedence effects and the evolution of chorusing. 32 Takahashi D.Y.

Fenley A.R.

Ghazanfar A.A. Early development of turn-taking with parents shapes vocal acoustics in infant marmoset monkeys. 32 Takahashi D.Y.

Fenley A.R.

Ghazanfar A.A. Early development of turn-taking with parents shapes vocal acoustics in infant marmoset monkeys. 33 Chow C.P.

Mitchell J.F.

Miller C.T. Vocal turn-taking in a non-human primate is learned during ontogeny. As few previous studies have attempted to examine anti-synchronized calling within a group [], it is unclear if there is an upper limit on the number of active participants in a vocal interaction governed by the principles discussed above. In humans, turn-taking in unsupervised group discussions was found to be challenging []. Additionally, in humans, factors such as turn allocation, gestures, and seniority [] likely play a central role. It has been stated that the basic organizational rules for spontaneous turn-taking “favor” only small groups of three or fewer participants and that larger groups require sequence organization [] or segmentation []. In contrast to this assertion, our results suggest that such patterns can be driven by a simple individual-level mechanism and can be efficiently maintained in unrestricted sender/receiver vocal interaction with well above three participants. Our results demonstrate that turn-taking in meerkats is not driven by simple neural resetting, as has been suggested for insect choruses []. It is also different from the coupled oscillator dynamics shown in common marmoset (Callithrix jacchus) and human turn-taking interactions []. The innate foundation of turn-taking [] and the suggested effects of social feedback and learning [] are important areas for future investigation.