1. Ecology
  2. Neuroscience
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Patterns of call communication between group-housed zebra finches change during the breeding cycle

  1. Lisa F Gill  Is a corresponding author
  2. Wolfgang Goymann
  3. Andries Ter Maat
  4. Manfred Gahr
  1. Max Planck Institute for Ornithology, Germany
Research Article
Cite this article as: eLife 2015;4:e07770 doi: 10.7554/eLife.07770
8 figures, 1 video, 3 tables and 1 data set

Figures

Figure 1 with 1 supplement
Position of on-bird microphones on freely behaving zebra finches.

Close-up pictures of backpacks fitted on zebra finches in an aviary. The visible white ‘backpack’ contains a microphone (at the bottom), a radio transmitter, and a battery. It is placed on the bird's back (centre of mass) in a way that the microphone faces inwards, that is, towards the bird's body. Unlike the backpacks, harnesses disappear under the birds' feathers (left and right panel and Video 1), therefore, to demonstrate how they were fixed on the birds, the two silicon loops around the head and the abdomen are represented by dashed lines in the left panel. They were closed at the front of the bird with a small knot.

https://doi.org/10.7554/eLife.07770.003
Figure 1—figure supplement 1
Group housing.

Overview of experimental room including aviary and technical set-up.

https://doi.org/10.7554/eLife.07770.004
Figure 2 with 1 supplement
Group reproductive stages change over time.

Percentage of birds (nbirds = 32) assigned to the seven detailed breeding stages (coloured bars) and the three corresponding condensed nest stages over the first 20 days of the trials. Earliest onset of nest material provisioning (day 7) is indicated by a green dashed vertical line. Source data are available at http://dx.doi.org/10.5061/dryad.vt69s.

https://doi.org/10.7554/eLife.07770.005
Figure 2—figure supplement 1
Differences in steroid hormone concentrations at baseline levels and the three nest stages.

Boxplots of (A) testosterone (TESTO), (B) dihydrotestosterone (DHT), and (C) progesterone (P4) concentrations with natural log-transformed values at baseline (Base) and the three nest stages Pre-, Early and Later Nesting, analysed separately for the 16 females (red, nBase = 16, nPre = 11, nEarly = 5, nLater = 13) and 16 males (blue, nBase = 15, nPre = 12, nEarly = 5, nLater = 12) from four trials. Bayesian estimates are plotted as coloured points, and 95% credible intervals as coloured lines. For an explanation of abbreviations, lines, and symbols, see Figure 4. For methods, detailed results and discussion of hormones in relation to nest stages see Appendix 1. Source data are available at http://datadryad.org/review?doi=doi:10.5061/dryad.vt69s.

https://doi.org/10.7554/eLife.07770.006
Call types used in our study.

Example spectrograms of female (A1) and male (A2) distance, tet (B), stack (C), cackle (D), and whine (E) calls. x-axis: time [ms], y-axis: frequency [Hz].

https://doi.org/10.7554/eLife.07770.007
Figure 4 with 1 supplement
Female and male call-type usage at different nest stages.

Boxplots of the number of vocalisations (natural log- or square-root transformed) per 4 hr of recordings for the different vocalisation types (A-E) in relation to the three Nest stages, analysed separately for females (red, nfemales = 12) and males (blue, nmales = 10) from the three trials. They show that call types change differently over Nest stages: distance calls decrease (A), and cackles (D) and whines (E) increase. Thick black horizontal line = median of observations, box = 25–75% quantile of the observations (length = interquartile range), whiskers = last observation within 1.5 times the interquartile range from the edge of the box, circles = observations farther than 1.5 time the interquartile range from the edge of the box, coloured point = fitted value (Bayesian estimate), coloured vertical bar = 95% credible intervals (CrI) of the fitted value. If Bayesian estimates (coloured points) and CrI (vertical coloured lines) do not overlap inside single plots, there is a difference in the number of vocalisations used in relation to Nest stage. Such differences are indicated by different letters at the top of each box. Sample sizes during Pre-, Early and Later Nest stage were: 24, 20, and 35 data points coming from 9, 10, and 12 females, and 23, 18, and 26 data points coming from 8, 8, and 10 males. Source data are available at http://datadryad.org/review?doi=doi:10.5061/dryad.vt69s.

https://doi.org/10.7554/eLife.07770.008
Figure 4—figure supplement 1
Changes in call repertoire at more detailed breeding stages.

Boxplots of the proportion of call types (y-axis) for females (top, nfemales = 12) and males (bottom, nmales = 10) over the detailed breeding stages (x-axis, UP: Unpaired, NN: No nest, Inspec: Nest inspection, Terr: Nest defence, Build: Nest building, Lay: Egg-laying, Incub: Incubation). Sample sizes during different breeding stages were 10, 14, 8, 12, 18, 10, and 7 data points coming from 7, 7, 6, 8, 12, 7, and 5 different females, and 10, 13, 6, 12, 15, 6, and 5 data points coming from 7, 6, 4, 8, 10, 5, and 3 different males. Bayesian estimates and CrI are plotted as coloured points and vertical bars (red: females, blue: males). For further explanations and abbreviations, see Figure 4. Note the different scale and missing Bayesian statistics for ‘whines’ (right), as these consisted a comparably small part of the repertoire and included many zero values, especially at the earlier breeding stages. A table showing all Bayesian estimates and credible intervals can be found in Appendix 2. Source data are available at http://datadryad.org/review?doi=doi:10.5061/dryad.vt69s.

https://doi.org/10.7554/eLife.07770.009
Figure 5 with 1 supplement
Vocal interactions within groups across reproductive stages.

(A) Vocal interaction matrices. Examples of vocal correlation indices (from −1 to 1, see colour scale) resulting from PSTHs for all bird and call-type combinations during different phases of the trials (different days indicated above each box), for trials I, II, and III (nbirds = 6, 8 and 8). All initiating birds (x-axis) and responding birds (y-axis) are represented by capital letters (pink: females, blue: males) and are subdivided into the five call types. Note that grey squares (= zero values) indicate there was no significant interaction in the respective dyad and does not mean there were no vocalisations (see ‘Materials and methods’). Same capital letters indicate members of a pair, and within-pair interactions can be found in the diagonal from top left to bottom right. Note an increase in within-pair interactions and a decrease in overall group interactions with progressing reproductive stages (left to right). Inserts in Figure 5A (lower right corner) explain the different interaction levels in the group (highlighted in pale blue) and the call-type interactions (highlighted in pale yellow). The dark grey diagonal from bottom left to top right represents within-bird interactions which were excluded from the analyses. Same-sex interactions are emphasized by pink (female–female) or blue (male–male) outer lines. In trial I, white squares represent missing values. The dataset is available at http://datadryad.org/review?doi=doi:10.5061/dryad.vt69s. (B) Within-pair vocal interactions at different breeding stages. Summary graph of positive within-pair calling interactions in relation to different call-type combinations, sex and the detailed breeding stages (npairs = 10). Initiating birds' call types are plotted on the x-axis and percentages of positive responses (pink: females, blue: males) are plotted on the y-axis, in the corresponding call types. Note that both females and males were initiating and responding birds. Source data are available at http://datadryad.org/review?doi=doi:10.5061/dryad.vt69s.

https://doi.org/10.7554/eLife.07770.010
Figure 5—figure supplement 1
Increasing specificity of within-pair vocal interactions.

Vocal activity (number of distance, tet, stack, cackle, and whine calls, green points = means, green lines = standard errors) and specificity of vocal interactions within pairs (red bars) and with non-pair members (grey bars) over the breeding stages (UP: Unpaired, NN: No nest, Inspec: Nest inspection, Terr: Nest defence, Build: Nest building, Lay: Egg-laying, Incub: Incubating). Note that the pair specificity of vocal interactions increased across breeding stages, and after birds had paired, they always shared more interactions with their partner than with other group members. Also note that for this graph, only trials II and III (n = 16 birds) were included due to the missing values in trial I (would allow investigation of within-pair interactions but not of vocal interactions from the entire colony). Sample sizes were thus 16, 25, 12, 14, 22, 12, and 10 observations coming from 10, 8, 8, 12, 16, 10, and 6 focal birds. Source data are available at http://datadryad.org/review?doi=doi:10.5061/dryad.vt69s.

https://doi.org/10.7554/eLife.07770.011
Call-type combinations associated with nest stages and successful egg-laying.

Boxplot of within-pair number of combinations with significant interaction (positive) over Pre- (nPre = 8), Early (nEarly = 8) and Later Nesting (nLater = 10) for pairs that were successful (orange, n = 6) and unsuccessful (grey, n = 4) at producing a clutch of eggs within the 3-week trials (Later Nest stage here refers only to Nest-building). Note the increase in call-type interactions of successful pairs across the Nest stages. Thick black horizontal line = median of observations, box = 25–75% quantile of observations (length = interquartile range), whiskers = last observation within 1.5 times the interquartile range the edge of the box, black dots = observations farther than 1.5 time the interquartile range from the edge of the box. Source data are available at http://datadryad.org/review?doi=doi:10.5061/dryad.vt69s.

https://doi.org/10.7554/eLife.07770.012
Synchronous external and on-bird recordings.

Example spectrograms (x-axis: time [ms], y-axis: frequency [kHz]) of synchronous recordings with (A) group recording from external microphone without individual information and (BD) individual recordings from three (out of eight) on-bird microphones. Dark vertical lines (in C and D) represent wing beats that hardly show up in the noisy external recording. Note the higher power in the low frequencies in the on-bird microphone recordings, compared to the external recording.

https://doi.org/10.7554/eLife.07770.015
Timeline of trials.

Timeline indicating housing conditions and approximate timing of backpack application, habituation phase (minimum 7 days), beginning of trial and sound recordings (ca. 3 weeks, see ‘Materials and methods’), onset of nest material availability, end of trial. Of the continuous sound recordings, mornings (220 ± 20 min) of different days (differed between trials, not indicated in graph) equally representing birds' breeding stages were analysed. Blood sampling occurred three times (indicated by red arrows): before the beginning of the trials, 1 day after males and females were joined and 1 day after nest material became available.

https://doi.org/10.7554/eLife.07770.016

Videos

Video 1
Zebra finches behaving freely with on-bird microphones.

Example video and external audio recording of Zebra finches behaving freely inside aviary (partial view) on the day of nest material. In the video, note the small white objects on the birds' backs (‘microphone backpacks’) that allow normal behaviours, for example, flight and collection of nest material. In the audio, note the soft, overlapping vocalisations, and wing beat sounds (see Figure 7).

https://doi.org/10.7554/eLife.07770.017

Tables

Table 1

Overview and short description of different agonistic, affiliative or sexual, and neutral behaviours and whether they were measured as occurrences (count) or every 2 min (duration)

https://doi.org/10.7554/eLife.07770.013
BehaviourDescriptionCount/DurationType
DisplacementFocal bird arrives at another bird's location forcing it to leaveCountAgonistic
FightingFor example, bill-fight, full body fight, chasingCount
ClumpingBirds sit in direct physical contact with each otherDurationAffiliative or sexual behaviour
AllopreeningOne bird preens another birdDuration
Copulation solicitationFemale fans tail at maleCount
CopulationMale mounts femaleCount
Enter nest boxBirds enter the same nest box without fightingCount
ForagingBird is foraging on ground, feeding, drinkingDurationNeutral
PreeningBird is self-preeningDuration
FlyingBird flies around in aviaryCount
IncubatingBird sitting inside nest box with eggsDuration
Table 2

Overview and short description of breeding stages and nest stages

https://doi.org/10.7554/eLife.07770.014
Breeding stageDescriptionNest stage
UnpairedBird does not show increased prosocial behaviour towards specific individualPre-nesting
No nestPaired but without nest
TerritorialPair defending nest site without nest materialEarly nesting
Nest inspectionPair inspecting different nest boxes
Nest buildingPair bringing nest material to nest boxLater nesting
LayingPair's female laying eggs
IncubationPair members incubating
Appendix 2—table 1

Bayesian estimates and credible intervals (CrI) for the proportion of call types in females and males in relation to the detailed Breeding stages

https://doi.org/10.7554/eLife.07770.018
FemalesMales
Call typeBreeding stageEstimateLower CrIUpper CrIEstimateLower CrIUpper CrI
DistanceUnpaired0.25700.18950.32180.24720.18180.3129
No nest0.12310.06290.18410.11330.05190.1765
Nest inspection0.0620−0.01510.13800.0522−0.02860.1293
Nest defence0.0565−0.00470.12020.0467−0.01500.1111
Nest building0.0351−0.01940.08950.0252−0.03080.0824
Egg-laying0.0335−0.03540.10480.0236−0.05020.1001
Incubation0.09200.01090.17120.0822−0.00140.1630
TetUnpaired0.20380.13980.26800.20380.13980.2680
No nest0.18200.12330.24090.18200.12330.2409
Nest inspection0.30730.22780.38880.30730.22780.3888
Nest defence0.10730.04640.16590.10730.04640.1659
Nest building0.13700.08260.19020.13700.08260.1902
Egg-laying0.09770.01890.17900.09770.01890.1790
StackIncubation0.09020.00230.18030.09020.00230.1803
Unpaired0.40610.26610.53930.12480.06360.1823
No nest0.22990.10340.35300.10400.04870.1620
Nest inspection0.37540.22120.52710.0695−0.00290.1444
Nest defence0.38400.25710.50970.09410.03810.1514
Nest building0.21330.10810.31510.06250.01090.1127
Egg-laying0.25800.12200.39240.16460.09670.2360
Incubation0.34930.17840.51830.09760.01660.1795
CackleUnpaired0.0409−0.06580.14630.1101−0.00760.2278
No nest0.22150.12880.31640.21140.09610.3258
Nest inspection0.21600.10250.33350.22780.08650.3613
Nest defence0.27710.17830.37290.28500.17210.3918
Nest building0.29140.21180.37670.34770.24220.4507
Egg-laying0.20020.09630.31020.20070.06310.3399
Incubation0.18770.06720.31260.0839−0.06740.2399

Data availability

The following data sets were generated
  1. 1

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