Early experience affects foraging behavior of wild fruit bats more than their original behavioral predispositions
- School of Zoology, Faculty of Life Sciences, Tel Aviv University, Israel
- Sagol School of Neuroscience, Tel Aviv University, Israel
Figures
Figure 1 with 1 supplement
Assessing personality in the laboratory.
(A) Schematic illustration of the experiments. (B) A 3D plot of the three behavioral traits, estimated during Trial 1. (C1-3) Behavioral traits were consistent over time. The behavioral traits of the first and third (post-enrichment) trial are presented. Positive correlations were found for all three behavioral traits over a period of more than 10 weeks. For the enriched (blue lines), the impoverished (orange lines), and both environments together (not shown), respectively: (C1) Boldness; (C2) exploration; and (C3) activity. (D) Boldness of the first and fifth (post-release 2) trial. Dashed line represents the Y=X line.
Figure 1—figure supplement 1
PCA analysis for trial 1 (baseline) and 5 (post-release 2); positive correlation was found between the individual scores on PC1 (Pearson correlation p=0.03, r=0.58).
Figure 2 with 1 supplement
Personality measurements over time.
(A) The behavioral traits of the first and second baseline trials, performed on two consecutive nights, are presented. Positive correlations were found for all three behavioral. Boldness (Pearson r=0.59, p=5.8e-05) (A1); exploration (Pearson r=0.70, p=5.3e-07) (A2); and activity (Pearson r=0.52, p=0.0005) (A3). Dashed line represents the Y=X line. (B) Box plots depicting the bats’ behavior across the five trials according to three traits: Boldness (B1), exploration (B2), and activity levels (B3). (C) Paired box plots show individual bat values in the first trial (baseline 1) and the fifth trial (post-release 144 days apart on average) for each trait: Boldness (C1), exploration (C2), and activity levels (C3). Lines connect repeated measurements from the same individual, illustrating within-individual behavioral changes over time. The number of bats participated in each trial is given in Methods, Table 8. In the baseline trials, no significant differences were found between the two environmental conditions (enriched / impoverished) for any of the three behavioral traits we measured (p=0.62, p=0.84, p=0.72 for boldness, exploration, and activity levels, respectively, n=40, Supplementary file 1). Figure 2—figure supplement 1 also shows the indication. The experimental phase and the time in days from the day of the first trial are depicted on the X-axis. Box plots show the 25% and 75% percentiles. Medians and whiskers based on 1.5 IQR are shown.
Figure 2—figure supplement 1
Full bat behavioral traits over time.
Box plots depicting the bats’ behavior across the five trials according to three traits: Boldness (A), exploration (B), and activity levels (C). The experimental phase and the time in days from the day of the first trial are depicted on the X-axis. Box plots show the 25% and 75% percentiles. Medians and whiskers based on 1.5 IQR are shown. A1, B1, and C1 represent all bats tested, while A2, B2, and C2 represent only the bats that were tracked outdoors using GPS devices. Note that Post Release 1 and Post Release 2 are identical in the left and right box plots.
Figure 3 with 2 supplements
Early environmental exposure affects outdoor foraging behavior.
(A1) Time spent by the bats outside the colony each night (in minutes). (A2). Distance to the furthest point from the colony per night. (A3) The area explored by the bats. The data for each bat were estimated for the period between its 15th and 20th days outdoors (n=17 bats). Median and whiskers based on 1.5 IQR are shown. (B–C) The complete movement of four individuals - two from each colony. (B) Individuals raised in the enriched colony, data shown for two individuals, each representing a different measured season (B1, B2); (C) Individuals raised in the impoverished colony, data shown for two individuals, each representing a different measured season (C1, C2). Colors depict time in days. The open colony is marked by a white circle. Insert in C1-2 zooms-in on the tracks. More examples of individual bat movement maps are presented in Figure 3—figure supplement 1.
Figure 3—figure supplement 1
Early environmental exposure affects outdoor foraging behavior.
The complete movement of four individuals - two from each colony. (A) Individuals raised in the enriched colony, data shown for two individuals (A1, A2); (B) Individuals raised in the impoverished colony, data shown for two individuals (B1, B2). Colors depict time in days. The open colony is marked by a white circle. Insert in B1 zooms-in on the tracks.
Figure 3—figure supplement 2
Early environmental exposure affects outdoor foraging behavior.
(A1) Time spent by the bats outside the colony each night (in minutes). (A2). Distance to the furthest point from the colony per night. (A3) The area explored by the bats. The data for each bat were estimated for the period between its 21st and 26th days outdoors (n=17 bats). Median and whiskers based on 1.5 IQR are shown.
Figure 4
Experimental set-up schematic.
Each bat is placed in a tent with six foraging boxes.
Author response image 1
Tables
Table 1
Pearson’s correlation test.
| Boldness 1–3 | Exploration 1–3 | Activity 1–3 | Boldness 1–5 | |
|---|---|---|---|---|
| Pearson r value | 0.66 | 0.66 | 0.51 | 0.6 |
| Pearson p-value | <9.7e-05 | 9.1e-0.5 | 0.004 | 0.021 |
Table 2
Mixed generalized linear model (GLM) results for the comparison between trials 1 and 5 response ~trial + (1 | bat ID).
| Response | AIC | BIC | LogLikelihood | Deviance | ||||
|---|---|---|---|---|---|---|---|---|
| Boldness | –36.379 | –28.498 | 22.189 | –44.379 | ||||
| Fixed effects coefficients (95% CIs) | ||||||||
| Name | Estimate | SE | tStat | DF | p-value | Lower | Upper | |
| Intercept | 0.408 | 0.031 | 13.16 | 51 | 5.03e-18 | 0.346 | 0.471 | |
| Trial number | 0.056 | 0.009 | 6.02 | 51 | 1.902e-07 | 0.037 | 0.075 | |
| Response | AIC | BIC | LogLikelihood | Deviance | ||||
| Exploration | 12.074 | 19.956 | –2.037 | 4.074 | ||||
| Fixed effects coefficients (95% CIs) | ||||||||
| Name | Estimate | SE | tStat | DF | p-value | Lower | Upper | |
| Intercept | 0.545 | 0.049 | 11.02 | 51 | 4.248e-15 | 0.446 | 0.644 | |
| Trial number | 0.018 | 0.016 | 1.157 | 51 | 0.252 | –0.013 | –0.013 | |
| Response | AIC | BIC | LogLikelihood | Deviance | ||||
| Activity | –580.34 | –572.46 | 294.17 | –588.34 | ||||
| Fixed effects coefficients (95% CIs) | ||||||||
| Name | Estimate | SE | tStat | DF | p-value | Lower | Upper | |
| Intercept | 0.002 | 0.0001 | 13.737 | 51 | 9.050e-19 | 0.002 | 0.003 | |
| Trial number | –0.0002 | 7.135e-05 | –4.065 | 51 | 0.0001 | –0.0004 | –0.0001 | |
Table 3
Mixed generalized linear model (GLM) results for all tested trials (1-5) response ~1 + Trial × EnvironmentalCondition + (1 | bat ID).
| Response | AIC | BIC | LogLikelihood | Deviance | ||||
|---|---|---|---|---|---|---|---|---|
| Boldness | –100.5 | –82.807 | 56.25 | –112.5 | ||||
| Fixed effects coefficients (95% CIs) | ||||||||
| Name | Estimate | SE | tStat | DF | p-value | Lower | Upper | |
| Intercept | 0.448 | 0.0444 | 10.078 | 137 | 3.266e-1 | 0.36 | 0.536 | |
| Environmental condition Impoverished | 0.007 | 0.061 | 0.117 | 137 | 0.906 | –0.115 | 0.129 | |
| Trial number | 0.038 | 0.014 | 2.744 | 137 | 0.006 | 0.010 | 0.066 | |
| Environmental condition Impoverished: Trial | –0.011 | 0.019 | –0.58 | 137 | 0.561 | –0.049 | 0.026 | |
| Response | AIC | BIC | LogLikelihood | Deviance | ||||
| Exploration | –0.46128 | 17.231 | 6.230 | –12.461 | ||||
| Fixed effects coefficients (95% CIs) | ||||||||
| Name | Estimate | SE | tStat | DF | p-value | Lower | Upper | |
| Intercept | 0.625 | 0.066 | 9.467 | 137 | 1.13e-16 | 0.494 | 0.755 | |
| Environmental condition Impoverished | –0.010 | 0.092 | –0.112 | 137 | 0.910 | –0.192 | 0.171 | |
| Trial number | –0.003 | 0.019 | –0.182 | 137 | 0.855 | –0.041 | 0.034 | |
| Environmental condition Impoverished:Trial | 0.0030.006 | 0.025 | 0.247 | 137 | 0.804 | –0.043 | 0.054 | |
| Response | AIC | BIC | LogLikelihood | Deviance | ||||
| Activity | –1586 | –1568.3 | 799.01 | –1598 | ||||
| Fixed effects coefficients (95% CIs) | ||||||||
| Name | Estimate | SE | tStat | DF | p-value | Lower | Upper | |
| Intercept | 0.002 | 0.0002 | 11.017 | 137 | 1.319e-2 | 0.002 | 0.003 | |
| Environmental condition Impoverished | 0.0002 | 0.0003 | 0.908 | 137 | 0.365 | –30e-5 | 0.0009 | |
| Trial number | –0.0002 | 7.292e-05 | –3.273 | 97 | 0.001 | –30e-3 | –9.e-05 | |
| Environmental condition Impoverished:Trial | –9.2e-05 | 9.640e-05 | –0.959 | 137 | 0.338 | –20e-5 | 9.8e-05 | |
Table 4
Mixed-effect generalized linear model (GLMM) results for outdoors measurements with the first boldness as predisposition.
The lines depicting results for the environmental and the predisposition effects are highlighted in green and blue, respectively. response ~1 + Environmental_condition + Baseline_boldness + Sex + Age + Days_spent_outside + (1 | Bat_ID).
| Response | AIC | BIC | Loglikelihood | Deviance | ||||
|---|---|---|---|---|---|---|---|---|
| Time spent outside | 8638.2 | 8674.8 | –4311.1 | 8622.2 | ||||
| Fixed effects coefficients (95% CIs) | ||||||||
| Name | Estimate | SE | tStat | DF | p-value | Lower | Upper | |
| Intercept | 185.42 | 74.081 | 2.469 | 710 | 0.013 | 38.014 | 332.83 | |
| Environmental condition Impoverished | –57.736 | 26.374 | –2.189 | 710 | 0.028 | –109.52 | –5.956 | |
| Boldness of the first baseline | –32.783 | 78.474 | –0.417 | 710 | 0.676 | –186.85 | 121.29 | |
| Bat sex Male | –9.0905 | 26.014 | –0.349 | 710 | 0.726 | –60.163 | 41.982 | |
| Bat age | 0.029 | 0.217 | 0.135 | 710 | 0.892 | –0.397 | 0.456 | |
| Number of days spent outside until assessment day | 1.416 | 0.351 | 4.028 | 710 | 6.10E-05 | 0.726 | 2.106 | |
| Response | AIC | BIC | Loglikelihood | Deviance | ||||
| Maximum distance per night | 12437 | 12474 | –6210.7 | 12421 | ||||
| Fixed effects coefficients (95% CIs) | ||||||||
| Name | Estimate | SE | tStat | DF | p-value | Lower | Upper | |
| Intercept | 1543.2 | 651.67 | 2.368 | 710 | 0.018 | 263.73 | 2822.6 | |
| Environmental condition Impoverished | –591.24 | 228.02 | –2.592 | 710 | 0.009 | –1038.9 | –143.57 | |
| Boldness of the first baseline | –550.64 | 649.03 | –0.848 | 710 | 0.396 | –1824.9 | 723.6 | |
| Bat sex Male | –262 | 224.84 | –1.165 | 710 | 0.244 | –703.43 | 179.42 | |
| Bat age | –0.705 | 1.888 | –0.372 | 710 | 0.708 | –4.414 | 3.002 | |
| Number of days spent outside until assessment day | 10.982 | 3.868 | 2.838 | 710 | 0.004 | 3.386 | 18576 | |
| Response | AIC | BIC | Loglikelihood | Deviance | ||||
| Explored area | 116.55 | 123.68 | –50.277 | 100.55 | ||||
| Fixed effects coefficients (95% CIs) | ||||||||
| Name | Estimate | SE | tStat | DF | p-value | Lower | Upper | |
| Intercept | –4.31 | 6.312 | –0.682 | 12 | 0.507 | –18.065 | 9.444 | |
| Environmental condition Impoverished | –5.286 | 2.081 | –2.539 | 12 | 0.025 | –9.821 | –0.75 | |
| Boldness of the first baseline | 7.746 | 6.454 | 1.2 | 12 | 0.253 | –6.315 | 21.809 | |
| Bat sex Male | –2.354 | 2.26 | –1.041 | 12 | 0.318 | –7.279 | 2.57 | |
| Bat latest age | 0.001 | 0.022 | 0.068 | 12 | 0.946 | –0.047 | 0.05 | |
| Total amount of nights the bat spent outside | 0.183 | 0.074 | 2.466 | 12 | 0.029 | 0.021 | 0.346 | |
Table 5
Mixed-effect generalized linear model (GLMM) results for outdoors measurements with the baseline trial PC1 as predisposition.
The lines depicting results for the environmental and the predisposition effects are highlighted in green and blue, respectively.
| Response | AIC | BIC | Loglikelihood | Deviance | ||||
|---|---|---|---|---|---|---|---|---|
| Time spent outside | 8636.9 | 8673.5 | –4310.4 | 8620.9 | ||||
| Fixed effects coefficients (95% CIs) | ||||||||
| Name | Estimate | SE | tStat | DF | p- value | Lower | Upper | |
| Intercept | 161.22 | 66.908 | 2.409 | 710 | 0.016 | 29.864 | 292.58 | |
| Environmental condition Impoverished | –58.829 | 26.251 | –2.241 | 710 | 0.025 | –110.37 | –7.289 | |
| PC1 of the first baseline | 0.619 | 54.32 | 0.011 | 710 | 0.990 | –106.03 | 107.27 | |
| Bat sex Male | –7.650 | 26.159 | –0.292 | 710 | 0.770 | –59.01 | 43.708 | |
| Bat age | 0.084 | 0.242 | 0.347 | 710 | 0.727 | –0.391 | 0.559 | |
| Number of days spent outside until assessment day | 1.347 | 0.379 | 3.547 | 710 | 0.0004 | 0.601 | 2.093 | |
| Response | AIC | BIC | Loglikelihood | Deviance | ||||
| Maximum distance per night | 12438 | 12474 | –6210.9 | 12422 | ||||
| Fixed effects coefficients (95% CIs) | ||||||||
| Name | Estimate | SE | tStat | DF | p-value | Lower | Upper | |
| Intercept | 1434.7 | 594.15 | 2.414 | 710 | 0.015 | 268.2 | 2601.2 | |
| Environmental condition Impoverished | –580.89 | 226.37 | –2.566 | 710 | 0.010 | –1025.3 | –136.46 | |
| PC1 of the first baseline | –365.17 | 460.75 | –0.792 | 710 | 0.428 | –1269.8 | 539.43 | |
| Bat sex Male | –318.9 | 225.1 | –1.416 | 710 | 0.157 | –760.83 | 123.03 | |
| Bat age | –1.108 | 2.121 | –0.522 | 710 | 0.601 | –5.274 | 3.057 | |
| Number of days spent outside until assessment day | 11.783 | 4.107 | 2.868 | 710 | 0.004 | 3.718 | 19.847 | |
| Response | AIC | BIC | Loglikelihood | Deviance | ||||
| Explored area | 117.82 | 124.94 | –50.909 | 101.82 | ||||
| Fixed effects coefficients (95% CIs) | ||||||||
| Name | Estimate | SE | tStat | DF | p-value | Lower | Upper | |
| Intercept | 1.331 | 5.878 | 0.226 | 12 | 0.824 | –11.476 | 14.139 | |
| Environmental condition Impoverished | –5.544 | 2.154 | –2.573 | 12 | 0.024 | –10.239 | –0.849 | |
| PC1 of the first baseline | –1.518 | 4.323 | –0.351 | 12 | 0.731 | –10.939 | 7.902 | |
| Bat sex Male | –1.712 | 2.274 | –0.752 | 12 | 0.465 | –6.668 | 3.242 | |
| Bat latest age | –0.005 | 0.025 | –0.217 | 12 | 0.831 | –0.061 | 0.050 | |
| Total amount of nights the bat spent outside | 0.174 | 0.077 | 2.243 | 12 | 0.044 | 0.005 | 0.343 | |
Table 6
Pearson correlation test results.
| Pearson r value | Pearson p-value | |
|---|---|---|
| Time spent out vs maximal distance | 0.28 | 0.23 |
| Time spent out vs explored area | 0.21 | 0.38 |
| Maximal distance vs explored area | 0.82 | <1.269e-05 |
Table 7
Egyptian Fruit bat pups were captured with their mothers in rural and urban colonies and then divided between two environmental conditions, enriched and impoverished.
| Season | Environmental condition | Colony ID | Coordinates | Number of pairs |
|---|---|---|---|---|
| 1 (2019–2020) | Enriched | Tinshemet | 31°59'43.2"N 34°57'19.2"E | 1 |
| Beit Guvrin | 31°36'45.8"N 34°53'41.7"E | 1 | ||
| Herzliya | 32°10'18.4"N 34°48'51.1"E | 4 | ||
| Impoverished | Tinshemet | 31°59'43.2"N 34°57'19.2"E | 1 | |
| Beit Guvrin | 31°36'45.8"N 34°53'41.7"E | 1 | ||
| Herzliya | 32°10'18.4"N 34°48'51.1"E | 3 | ||
| 2 (2020–2021) | Enriched | Beit Guvrin | 31°36'45.8"N 34°53'41.7"E | 5 |
| Herzliya | 32°10'18.4"N 34°48'51.1"E | 9 | ||
| Impoverished | Beit Guvrin | 31°36'45.8"N 34°53'41.7"E | 5 | |
| Herzliya | 32°10'18.4"N 34°48'51.1"E | 10 |
Table 8
Number of bats that participated in each of the trials.
| Environmental condition | Baseline (both 1+2) | Post-enrichment trial | Post-release trials (4+5) | |
|---|---|---|---|---|
| Season 1 | Enriched | 6 | - | 4 |
| Impoverished | 5 | - | 5 | |
| Season 2 | Enriched | 13 | 14 | 5 |
| Impoverished | 15 | 15 | 5 | |
| Total number of bats | 39 | 29 | 19 |
Table 9
Full timeline of the experiment.
| October-December | December-June | |||||
|---|---|---|---|---|---|---|
| 2019–2020 | Baseline Trials n=11 | Environmental enrichment | Release to open colony | Tracking bats using GPS devices n=10 | Post-release trials n=9 | |
| 2020–2021 | Baseline Trials n=29 | Environmental enrichment | Post-enrichment trial n=29 | Release to open colony | Tracking bats using GPS devices n=11 | Post release trials n=10 |
Additional files
-
Supplementary file 1
Mixed generalized linear model (GLM) results for baseline trials of two environmental conditions response ~1 + Environmental_condition + Trial_number + (1| Bat_ID).
- https://cdn.elifesciences.org/articles/103220/elife-103220-supp1-v1.docx
-
Supplementary file 2
Mixed-effect generalized linear model (GLMM) results for proportion of nights foraging outside the roost (%).
DaysOutProportion ∼1 + EnvironmentalCondition + Sex + Age + (1∣Bat_ID) With Y ∼ Binomial (TotalExperimentDays) and link = logit.
- https://cdn.elifesciences.org/articles/103220/elife-103220-supp2-v1.docx
-
MDAR checklist
- https://cdn.elifesciences.org/articles/103220/elife-103220-mdarchecklist1-v1.pdf
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Early experience affects foraging behavior of wild fruit bats more than their original behavioral predispositions
eLife 14:RP103220.
https://doi.org/10.7554/eLife.103220.3
