Research ArticleECOLOGY

Habituation is not neutral or equal: Individual differences in tolerance suggest an overlooked personality trait

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Science Advances  08 Jul 2020:
Vol. 6, no. 28, eaaz0870
DOI: 10.1126/sciadv.aaz0870
  • Fig. 1 FID procedure and measurements.

    This highlights the distance variables that can be measured as a function of the focal animal’s behavioral responses. Start distance (SD), visual orientation distance (VOD), VOD delay (VODD), VOD interval (VODI), flight initiation distance (FID). Adapted from (57).

  • Fig. 2 Conditional effect plots for interaction between observer identity and individual trial number per observer from VOD and FID models.

    The plot represents conditional predictions of the regression curve when all fixed effects are held constant apart from the interaction (observer × individual trial number per observer); the mean was used as the measure of central tendency, with the shaded areas displaying the relevant credible intervals (2.5 and 97.5% percent quantiles). AA represents the familiar observer, and AB represents the unfamiliar observer.

  • Fig. 3 Convergent validity regression.

    Regression relationship between visual tolerance and displacement tolerance. Estimates were derived from bivariate Bayesian model; lower values indicate greater “tolerance.” Each point represents the conditional modes of an individual baboon (n = 69) for each tolerance trait.

  • Table 1 Factors hypothesized to influence VOD and FID in baboons.

    Contextual variables that could be major drivers of VOD and FID responses in habituated chacma baboons (examples from relevant literature supporting the inclusion of each hypothesis can be found in table S1).

    FactorsLink to sensory capacity/FID/personality
    Response variable: VOD
    Observer (pseudo-predator) identity, X1Unfamiliar observer considered a greater threat, leading to increased risk
    perception and tendency to visually orient, resulting in longer VOD
    Trial number, X2(i) Increase or decrease in VOD with trial number indicative of habituation or
    sensitization (respectively) to FID approach methodology
    (ii) Consistent individual VOD response through time indicates personality trait.
    Compatibility: Not engaged (looking/not looking),
    engaged (not looking), X3
    Looking may enable animals to collect multiple types of information
    concurrently; in addition, being “not engaged” may afford focal animals a
    greater sensory capacity for detection. As a result, individuals looking as
    approach commences will visually orient toward approaching observer
    sooner resulting in longer VOD; engaged should yield shorter VOD.
    Habitat (open/closed), X4(i) “Open” habitats may afford individuals greater visibility, increasing
    likelihood of attending to approaching observer quicker, resulting in
    longer VOD.
    (ii) Open habitats are generally considered safer for baboons, as they permit
    earlier detection and avoidance of predators; therefore, risk perception
    could be lower, reducing tendency to visually orient toward approaching
    observer, resulting in shorter VOD.
    (iii) Open habitats may increase risk perception, as focal animals are less
    concealed from potential threats, increasing tendency to visually orient
    toward approaching observer, resulting in longer VOD.
    (iv) Open habitats have lower refuge availability, which may increase risk
    perception, resulting in longer VOD.
    Height (ground/above ground), X5“Above ground” may afford individuals greater visibility, resulting in longer
    VOD. In this context, above ground is <50 cm from ground level and is
    unlikely to qualify as potential refuge and therefore should not influence
    risk perception.
    Number of neighbors within 5 m, X6(i) As number of neighbors increase, the likelihood of a neighbor visually
    orienting toward the approacher increases, i.e., collective detection, which
    could result in longer VOD.
    (ii) As number of neighbors increase, the likelihood of predation decreases
    reducing risk perception and the tendency to visually orient toward the
    approach observer, resulting in shorter VOD.
    (iii) Increasing number of neighbors may mask both the visual and audible
    cues associated with the observer’s approach, resulting in shorter VOD,
    e.g., neighbors draw visual attention away from observer or noises from
    neighbors mask the sounds of observer’s footsteps during approach.
    Neighbor flight, X7Local conspecifics initiating flight before the focal animal will increase risk
    perception and evoke vigilance. Both factors could lead to focal animals
    visually orienting toward approaching observer sooner, resulting in
    longer VOD.
    External factors (local alarms, aggressions within 5 min), X8Localized threatening stimuli lead to increased risk perception and tendency
    to visually orient, resulting in longer VOD.
    Localized visual and audible stimuli may reallocate some of the focal animal’s
    finite attention, resulting in longer VOD.
    Response variable: FID
    VODI, X9When visual orientation interval (distance between VOD and FID) is long,
    focal animals will flee sooner, resulting in longer FID.
    Engaged/Not engaged, X10FID will be higher if focal animal was engaged at the start of the approach, as
    flight costs are higher because of interrupted social time (i.e., grooming)
    or loss of food patch (i.e., foraging).
    Observer (pseudo-predator) identity, X1Unfamiliar observer is considered a greater threat; therefore, FID should be
    greater for unfamiliar observer
    Trial number, X2(i) Increase or decrease in FID with trial number indicative of sensitization or
    habituation (respectively) to FID approach methodology
    (ii) Consistent FID response through time indicates personality trait.
    Habitat (open/closed), X4(i) Open habitats are generally considered safer for baboons, as they permit
    earlier detection and avoidance of predators; therefore, risk perception
    could be lower, resulting in shorter FID.
    (ii) Open habitats may increase risk perception, as focal animals are less
    concealed from potential threats, resulting in longer FID.
    (iii) Open habitats have lower refuge availability, which may increase risk
    perception, resulting in longer FID.
    Number of neighbors within 5 m, X6(i) Risk diluted with greater number of neighbors; therefore, FID should
    decrease as number of neighbors increases.
    (ii) Increasing number of neighbors increases localized visual and audible
    stimuli and therefore may reallocate some of the focal animal’s finite
    attention resulting in decreased FID.
    Neighbor flight, X7Local conspecifics initiating flight before the focal animal will increase risk
    perception and therefore increase FID.
    External factors (local alarms, aggressions within 5 min), X8(i) Localized threatening stimuli leads to increased risk perception and
    therefore increased FID.
    (ii) Localized visual and audible stimuli may reallocate some of the focal
    animal’s finite attention therefore decreasing FID.
  • Table 2 Responses by baboons to approach and hypothesized meaning.

    Hypothesized individual baboon behavioral response to human approaches and the threat level these responses are considered equivalent to.

    Observer considered:Equivalent to
    predator
    Equivalent to social
    threat
    Minimal threatNo threatNo. of observations
    (percentage of total
    observations)
    Response predictor
    Alarm barkY0 (0%)
    Flight direct to refuge
    (rocks, trees, or cliff)
    Y0 (0%)
    Rapid flight/sprinting
    response
    YY0 (0%)
    Displacement with geck/
    grimace
    Y16 (0.97%)
    Animal passively
    displaces
    YY1637 (98.85%)
    Flinch/startled before
    flight*
    –/*–/*–/*–/*3 (0.18%)
    Animal is not displaced–/*Y0 (0%)
    Animal is not displaced
    and threatens
    observer
    Y0 (0%)

    *Flinch or startled suggests that the focal animal detected observer within its usual tolerance level.

    • Table 3 VOD model summary.

      Parameter estimates for the model describing the relationship between VOD and the predictor variables. CI, credible interval.

      Population-level effects
      EstimateEst. error1–95% CIU-95% CIRhatBulk_ESSTail_ESS
      Intercept1.060.080.91.221.0023,28935,333
      VODD−0.020.01−0.0301.0034,76041,624
      Looking0.210.020.170.251.0069,33746,658
      Not engaged not looking0.110.020.060.161.0070,82147,802
      Open (Habitat)0.150.020.120.191.0073,74846,813
      Ground (Height)0.060.05−0.040.161.0074,86545,743
      Number of neighbors−0.050.01−0.06−0.031.0076,91046,466
      Neighbor flee first0.080.0400.161.0078,00346,586
      External factors within 5 min0.020.03−0.040.081.0079,04547,160
      Unfamiliar observer (AB)−0.040.07−0.190.111.0017,01128,032
      Trial number−0.010.01−0.020.011.0018,35129,277
      Unfamiliar observer (AB): Trial number0.010.01−0.010.031.0017,13826,376
      Family specific (log-normal)
      Sigma0.310.010.30.321.0048,39743,998
      Group-level effects
      Date (58 levels)
      sd(Intercept)0.140.020.10.181.0017,02732,825
      Individual identity (69 levels)
      sd(Intercept)0.240.030.180.311.0013,55827,638
      sd(VODD)0.040.010.020.051.0019,66331,617
      sd(ObserverAB)0.090.040.010.171.007,95613,090
      sd(TrialNo)0.01000.021.007,99511,891
      sd(ObserverAB:TrialNo)0.010.0100.021.005,45412,200
      cor(Intercept,VODD)0.570.190.150.891.0014,07124,184
      cor(Intercept,ObserverAB)0.210.31−0.460.761.0025,09133,269
      cor(VODD,ObserverAB)0.160.33−0.530.741.0020,67133,171
      cor(Intercept,TrialNo)−0.680.22−0.94−0.11.0022,28921,411
      cor(VODD,TrialNo)−0.30.29−0.80.321.0017,87527,326
      cor(ObserverAB,TrialNo)−0.170.37−0.810.571.0017,56930,321
      cor(Intercept,ObserverAB:TrialNo)0.350.3−0.370.821.0018,44921,803
      cor(VODD,ObserverAB:TrialNo)0.290.31−0.410.81.0027,31529,181
      cor(ObserverAB,ObserverAB:TrialNo)−0.050.39−0.720.721.0017,70533,765
      cor(TrialNo,ObserverAB:TrialNo)−0.470.34−0.910.41.009,75521,676
    • Table 4 FID model summary.

      Parameter estimates for the model describing the relationship between FID and the predictor variables.

      Population-level effects
      EstimateEst. Error1–95% CIU-95% CIRhatBulk_ESSTail_ESS
      Intercept0.670.10.470.871.0013,55628,565
      VODI−0.040.01−0.07−0.011.0045,43645,243
      Engaged0.140.020.10.181.0097,77646,015
      Open (Habitat)0.120.020.080.161.0091,77547,949
      Ground (Height)0.120.0600.231.00100,35148,107
      Number of neighbors−0.080.01−0.09−0.061.0098,90947,398
      Neighbor flee first00.05−0.090.091.0094,50045,544
      External factors within 5 min0.010.04−0.060.081.0094,48745,998
      Unfamiliar observer (AB)−0.140.08−0.30.031.0019,46330,667
      Trial number−0.020.01−0.04−0.011.0021,54234,353
      Unfamiliar observer (AB): Trial
      number
      0.020.0100.051.0017,99627,736
      Family specific (log-normal)
      Sigma0.360.010.340.371.0055,46945,557
      Group-level effects
      Date (58 levels)
      sd(Intercept)0.140.020.110.191.0017,30031,725
      Individual identity (69 levels)
      sd(Intercept)0.490.050.40.61.0013,78025,841
      sd(VODI)0.060.020.020.091.0010,33813,826
      sd(ObserverAB)0.180.040.10.261.0017,27616,843
      sd(TrialNo)0.01000.021.0011,64313,855
      sd(ObserverAB:TrialNo)0.010.0100.021.008,88018,037
      cor(Intercept,VODI)0.260.22−0.160.71.0022,51825,743
      cor(Intercept,ObserverAB)0.040.2−0.330.441.0034,50635,920
      cor(VODI,ObserverAB)0.160.28−0.390.681.0010,04818,984
      cor(Intercept,TrialNo)−0.460.25−0.840.151.0043,02829,416
      cor(VODI,TrialNo)−0.250.33−0.810.451.0017,51928,304
      cor(ObserverAB,TrialNo)−0.390.29−0.860.261.0021,98231,250
      cor(Intercept,ObserverAB:TrialNo)−0.120.33−0.730.561.0045,30339,936
      cor(VODI,ObserverAB:TrialNo)−0.360.35−0.880.471.0026,56934,646
      cor(ObserverAB,ObserverAB:TrialNo)−0.050.37−0.70.691.0031,43941,766
      cor(TrialNo,ObserverAB:TrialNo)−0.130.39−0.770.671.0019,03735,675

    Supplementary Materials

    • Supplementary Materials

      Habituation is not neutral or equal: Individual differences in tolerance suggest an overlooked personality trait

      Andrew T. L. Allan, Annie L. Bailey, Russell A. Hill

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      • Tables S1 to S3
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