Research ArticleEVOLUTIONARY BIOLOGY

Vocalizing in chimpanzees is influenced by social-cognitive processes

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Science Advances  15 Nov 2017:
Vol. 3, no. 11, e1701742
DOI: 10.1126/sciadv.1701742
  • Fig. 1 Experiment 1 setup and predictions: Chimpanzee behavior while seeing a snake model.

    We placed a partially hidden snake model (fig. S1) along the anticipated travel path of a subject. We tested whether marking behavior took the visual perspective of receivers into account (whether the receiver could see a snake model). Black chimpanzee, subject’s position and orientation with respect to the snake model and receivers; gray chimpanzee, the receiver’s position and orientation. Behavior of the subjects upon seeing the snake when both arrive from the left side: (A) Subject’s attention is snake-focused. (B) Marking, strictly defined as repositioning oneself to have direct visual access to both the snake and the receiver and to alternate gaze between the snake and the receiver. Gaze alternation was defined as head-turning between the receiver and the snake without intervening looks in other directions. Receivers were defined as having seen the snake once they had an unobstructed view to the model. (C) The subject leaves the snake. Predictions: H1 (receiver knowledge), the subjects engage in an initial phase of (A) but rapidly switch to (B). The subjects only switch from (B) to (C) once the subjects have seen that the receivers see the snake. H2 (signaler habituation), the subjects engage in (A) and (C) only. H3 (receiver identity), the subjects are more likely to engage in (B) if at least one receiver is a bond partner. H4 (receiver behavior), the subjects are more likely to stop engaging in (B) when the subjects see that the receivers are no longer at risk, such as when leaving the snake. Green line, trail; log, hiding snake model; snake model, gaboon or rhinoceros viper.

  • Fig. 2 Experiment 2 setup and illustration of the results: A two-stimulus design where chimpanzees first hear a playback and then see a snake model.

    Arrow thickness indicates chimpanzees’ level of attention. Speak bubbles represent number of calls and rate of calling. (A and B) Presentation of stimulus 1. (C and D) Presentation of stimulus 2. The subject walks along a path and hears a playback of either a rest hoo (A) or an alert hoo (B), simulating a receiver. The subjects hearing a threat-related call (an alert hoo) looked more to the speaker than after hearing a rest hoo, a call not associated with threats. After reacting to the speaker, the subjects then continued walking and then saw a snake model hidden behind a log, some seconds after hearing the playback of a hoo. No further receiver behavior is presented. We asked: Does the subjects’ behavior change upon seeing the snake in a way that is consistent with them monitoring in the receivers’ perspective? (C) In the rest hoo condition (receiver-ignorant), consistent with the subjects keeping track of the receivers’ perspective, the subjects persisted in monitoring the speaker and were highly likely to call and mark the position of the snake. (D) In contrast, in the alert hoo condition (receiver-knowledgeable), the subjects dropped interest in monitoring the speaker, and called and marked little. Slower calling rate in (C) compared to (D) is better explained by the receiver knowledge than the signaler habituation hypothesis. There was no change in attention given to the snake across conditions. In the absence of visual cues, it appears that the subjects not only monitored the receivers’ awareness of a threat but also changed their communication depending on the receivers’ awareness of the threat. Green line, trail; box, speaker hidden behind vegetation; snake model, gaboon or rhinoceros viper hidden behind a small log. Relative distances at the time of playback were 5 to 10 m between the subject and the speaker, the subject and the snake, and the speaker and the snake.

  • Fig. 3 Experiment 1: Subjects’ marking at a snake model is influenced by the receivers’ perspective and influences receivers’ responses.

    (A) Relative duration of the subjects’ marking: before (mark 1) and after (mark 2) receivers have seen the snake. Dots joined by dashed lines, data per subject averaged across trials. Mark 1 + mark 2 = total marking time. Inspect, duration over which the subjects’ attention remains snake-focused before engaging in marking (mean ± SD, 24 ± 13 s; range, 10 to 46 s; marking defined in Fig. 1). Mark 1, duration from the beginning of marking until the receiver sees the snake (mean ± SD, 55 ± 42 s; range, 7 to 140 s). Mark 2, duration over which marking continues after the receiver has seen the snake until the subject leaves snake or no longer looks to the snake (mean ± SD, 15 ± 6.3 s; range, 4 to 22 s). Darker dots, more data points per value. *P < 0.05, ***P ≤ 0.001. Model significance versus the null model: χ² = 12.99, df = 2, P = 0.002, n = 8 subjects, 10 cases, and 7 events. GLMM estimates: inspect versus mark 1: β = 0.58, SE = 0.26, t = 2.25, P = 0.03; mark 2 versus mark 1: β = 1.07, SE = 0.26, t = 4.15, P = 0.0003; inspect versus mark 2: β = −0.49, SE = 0.26, t = −1.89, P = 0.067. (B) Marking cessation with respect to receiver behavior (first bar) or when receiver sees the snake (second bar); y axis, proportion of cases. The bars show the subjects that stopped marking after witnessing the following receiver behavior: left bar (risk-reducing behavior): white, leave the snake (not risk-reducing behavior); light gray, still approaching the snake; dark gray, closest approach to the snake; black, no movement during marking; right bar: black, subjects stop marking after receiver sees the snake; 14 cases from n = 10 subjects (8 events). (C) The receivers’ behavior toward the snake depends on the subjects’ signaling. n = 37 cases, 22 subjects (12 events). Table 1C shows the test result. Three bars show the differential signaling of subjects: no signal, call or mark (calling, n = 8; marking, n = 2), and call and mark. Blocks of color indicate different receiver behaviors with respect to the snake model after the subjects’ signaling behavior. Approach, cautious approach to see a snake model; avoid, a detour of >5 m around the snake; pass 1 m, pass within the biting range of snake model—apparently unaware of the snake; passed, receiver had either already passed the snake or did not change position while the subject could see the snake model.

  • Fig. 4 Experiment 2: Subject’s signaling behavior toward the snake model differed depending on experimental conditions—the playback stimulus heard previously.

    (A to D) Comparison of response to alert versus rest hoo stimulus. Dots joined by dashed lines, data per subject averaged across trials within conditions. Larger dots, more data points per value. *P < 0.1, **P < 0.05, ***P < 0.01. Bar plot shows mean + SD with 95% confidence interval. GLMM results are shown in Table 2. n = 10 subjects, 21 trials, and 12 dyads. Note that sample sizes and thus statistical power in (B) and (C) are particularly small, because only cases where calling occurred could be included; x axis, experimental condition (playback stimulus played). (E) Speaker-directed scans after the playback before seeing the snake. (F) Post/prior speaker-directed scans comparing subjects’ scans after seeing the snake with those before seeing the snake.

  • Table 1 Experiment 1: Chimpanzee marking behavior at snake models with respect to receivers.

    Experiment 1: Chimpanzee marking behavior at snake models with respect to receivers.. (A and B) The likelihood of subjects to initiate marking. (C) The impact of signal type on receiver behavior. Binomial GLMMs: Marking, reposition oneself to see both the snake and the receiver and gaze alternate between the snake and the receiver. H1, receiver has seen the snake before signaler calls or marks (yes/no); H2, subject is first to see the snake (yes/no); H3, receivers include a bond partner (yes/no); H4, subjects could see or hear receivers approaching when first to see the snake. Random factors include subject identity and event. Bold: P < 0.05. Model significance versus null model built of control predictors (for H2 to H4) and random effects: (A) χ² = 9.91, df = 1, P = 0.002; (B) χ² = 4.2, df = 1, P = 0.038. n = 37 cases, 22 subjects, and 12 snake placement events. We conducted two models instead of one due to model stability issues with four predictor variables. After running model (A), we removed the nonsignificant variable, replaced it with the remaining predictor variable, and reran the model [model (B)]. All significant variables remain significant with a Bonferroni correction [required across models (A) and (B)]. Model (C) included only receivers who had not seen the snake. n = 27 cases, 17 subjects, and 12 events: χ² = 6.41, df = 1, P = 0.011. See table S1 for the source data.

    Predictor variableβSEχ²P
    A. Response variable: mark (yes)
    Intercept11.609.80
    H1: Receiver knowledge: receiver has seen the snake (no)21.3410.49.910.002
    H2: Habituation: subject is first to see the snake (yes)−1.775.700.070.70
    H3: Receiver identity: bond partner present (yes)19.988.1311.600.001
    B. Response variable: mark (yes)
    Intercept10.767.20
    H1: Receiver knowledge: receiver has seen the snake (no)19.137.204.280.008
    H3: Receiver identity: bond partner present (yes)20.488.9813.450.022
    H4: Receiver behavior: receivers approaching (yes)2.015.720.140.73
    C. Response variable: receiver behavior cautious approach (yes)
    Intercept0.410.91
    Mark and call (yes)2.601.136.440.011
    Call (yes)−0.691.220.320.57
  • Table 2 Experiment 2: Subjects’ vocal, nonvocal, and monitoring behavior at snake models is best explained by the receiver knowledge, not signaler habituation, hypothesis.

    Experiment 2: Subjects’ vocal, nonvocal, and monitoring behavior at snake models is best explained by the receiver knowledge, not signaler habituation, hypothesis.. Subjects’ overall responses across all tests differed significantly across conditions (permutation test correcting for multiple testing: χ² = 62.47, P = 0.004). Parentheses denote the variable level that reflects the estimate when tested against the alternative level. GLMMs: H1 (receiver knowledge), supported or tentatively supported by models (B) to (H); H2 (signaler habituation), not supported by models (B) to (H). n = 10 subjects, 21 trials, and 12 dyads. Bold: P < 0.05; italic, P < 0.1. Test predictor for all models, experimental condition (rest hoo and alert hoo). Random factors for all models include subject identity, dyad identity of subject, and call provider. Binomial, models (B), (E), and (F); Gaussian, models (A), (C), (D), and (G) to (I). Model significance versus null model, effect size (marginal R2): (A) χ² = 10.31, df = 1, P = 0.006; R2 = 0.16; (B) χ² = 6.7, df = 1, P = 0.009; (C) χ² = 3.12, df = 1, P = 0.077; R2 = 0.30; (D) χ² = 3.96, df = 1, P = 0.046; R2 = 0.32; (E) variable “alone” excluded due to model stability: χ² = 7.89, df = 1, P = 0.005; (F) χ² = 9.9, df = 1, P = 0.002; (G) χ² = 6.4, df = 1, P = 0.25; R2 = 0.26; (H) χ² = 2.65, df = 1, P = 0.10; R2 = 0.17; (I) χ² = 6.9, df = 1, P = 0.0085; R2 = 0.41. For models (C) and (D), cases containing zeros were excluded; thus, P values are likely affected by low power (see Fig. 4, C and D, for paired data plots, table S2 for source data, and table S4 for additional analyses of control variables).

    Response variablePredictor variableβSEχ²PH1H2
    Calling and marking behavior
    A. Number of calls emitted*Intercept0.620.27
    Condition (rest hoo)0.560.186.730.009YesYes
    Alone (yes)0.030.380.010.94
    B. Call or notIntercept11.238.08
    Condition (rest hoo)15.0310.283.030.082(Yes)No
    Number of alert hoos played−0.132.970.0020.97No
    C. Latency to first call*Intercept1.660.41
    Condition (rest hoo)0.850.463.120.077(Yes)No
    Alone (yes)−0.770.432.880.090
    D. Median inter-call interval*Intercept8.655.96
    Condition (rest hoo)12.666.653.960.046YesNo
    Alone (yes)−9.126.282.430.12
    E. Call and mark co-occurrenceIntercept−10.836.02
    Condition (rest hoo)20.288.337.890.005YesNo
    F. Mark or notIntercept−10.05.14
    Condition (rest hoo)20.107.729.860.009YesNo
    Alone (yes)−0.264.900.0030.96
    Attentional state
    G. Scans to speaker/s: Post/prior seeing the snakeAlone (yes)0.500.20
    Condition (rest hoo)0.460.166.420.011YesNo
    Alone (yes)−0.250.280.770.38
    H. Looking duration to the snake before first looking awayIntercept1.770.22
    Condition (rest hoo)0.380.252.650.11NoNo
    Alone (yes)−0.240.251.100.30
    I. Scans to speaker/s after playback before the snakeIntercept0.530.086.910.009
    Condition (rest hoo)0.260.08
    Alone (yes)0.170.092.600.107

    *Transformation, log + 1.

    †Confirms results of previous study but does not discriminate between hypotheses.

    Supplementary Materials

    • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/3/11/e1701742/DC1

      video S1. Western chimpanzees (Pan troglodytes verus) in the Tai National Park, Ivory Coast, see real, highly camouflaged rhinoceros viper (www.youtube.com/watch?v=AVXU9C-Oq2k; see fig. S3 for stills).

      video S2. Experiment 1 with marking: Kato alert hoos and marks a gaboon viper model for an ignorant receiver with whom he shares a bond (Pan troglodytes schweinfurthii, Budongo Forest, Uganda).

      video S3. Experiment 1 without marking: Squibbs alert hoos but does not mark a gaboon viper model for ignorant receivers with whom he does not share a bond (P. troglodytes schweinfurthii, Budongo Forest, Uganda).

      video S4. Experiment 2: Rest hoo condition (P. troglodytes schweinfurthii, Budongo Forest, Uganda).

      video S5. Experiment 2: Alert hoo condition (P. troglodytes schweinfurthii, Budongo Forest, Uganda).

      Supplementary Methods

      table S1. Source data for experiment 1: Marking behavior in relation to test and control variables.

      table S2. Source data for experiment 2: Vocal and nonvocal behaviors of subjects per trial after seeing a snake model.

      table S3. Experiment 2: Predictions for receiver knowledge (H1) and signaler habituation (H2) hypotheses.

      table S4. Experiment 2: Control predictors have little influence on chimpanzee calling and marking behavior.

      fig. S1. Typical scenario upon viper (B. rhinoceros) detection by chimpanzees.

      fig. S2. Vipers photographed in the Budongo Forest and replica snake models used in the experiments.

      References (5255)

    • Supplementary Materials

      This PDF file includes:

      • Legends for videos S1 to S5
      • Supplementary Methods
      • table S1. Source data for experiment 1: Marking behavior in relation to test and control variables.
      • table S2. Source data for experiment 2: Vocal and nonvocal behaviors of subjects per trial after seeing a snake model.
      • table S3. Experiment 2: Predictions for receiver knowledge (H1) and signaler habituation (H2) hypotheses.
      • table S4. Experiment 2: Control predictors have little influence on chimpanzee calling and marking behavior.
      • fig. S1. Typical scenario upon viper (B. rhinoceros) detection by chimpanzees.
      • fig. S2. Vipers photographed in the Budongo Forest and replica snake models used in the experiments.
      • References (52–55)

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      Other Supplementary Material for this manuscript includes the following:

      • video S1 (.mp4 format). Western chimpanzees (Pan troglodytes verus) in the Tai National Park, Ivory Coast, see real, highly camouflaged rhinoceros viper (www.youtube.com/watch?v=AVXU9C-Oq2k; see fig. S3 for stills).
      • video S2 (.mp4 format). Experiment 1 with marking: Kato alert hoos and marks a gaboon viper model for an ignorant receiver with whom he shares a bond (Pan troglodytes schweinfurthii, Budongo Forest, Uganda).
      • video S3 (.mp4 format). Experiment 1 without marking: Squibbs alert hoos but does not mark a gaboon viper model for ignorant receivers with whom he does not share a bond (P. troglodytes schweinfurthii, Budongo Forest, Uganda).
      • video S4 (.mp4 format). Experiment 2: Rest hoo condition (P. troglodytes schweinfurthii, Budongo Forest, Uganda).
      • video S5 (.mp4 format). Experiment 2: Alert hoo condition (P. troglodytes schweinfurthii, Budongo Forest, Uganda).

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