Close-range vocal interaction in the common marmoset (Callithrix jacchus)

Abstract

Vocal communication in animals often involves taking turns vocalizing. In humans, turn-taking is a fundamental rule in conversation. Among non-human primates, the common marmoset is known to engage in antiphonal calling using phee calls and trill calls. Calls of the trill type are the most common, yet difficult to study, because they are not very loud and uttered in conditions when animals are in close proximity to one another. Here we recorded trill calls in captive pair-housed marmosets using wearable microphones, while the animals were together with their partner or separated, but within trill call range. Trills were exchanged mainly with the partner and not with other animals in the room. Animals placed outside the home cage increased their trill call rate and uttered more trills in response to their partner compared to strangers. The fundamental frequency, F0, of trills increased when animals were placed outside the cage. Our results indicate that trill calls can be monitored using wearable audio equipment and that minor changes in social context affect trill call interactions and spectral properties of trill calls.

Fig 1

A. Illustration of the experimental conditions with Animal A as the focal animal. B. A cartoon example of a typical room layout and positioning of the cages. The large rectangle is the room and the small rectangles represent cages. Each single cage has two marmosets. For families, two single cages are connected to make one large cage. The cage with dashed line is the home cage recorded from. The transport cage is in front of the home cage. During separation, one animal was placed in the transport cage. C. Photos of a marmoset wearing a jacket with a voice recorder mounted at the chest. The green patch on the back is for video identification purposes.

Fig 2. Audio signal strength versus distance.

A. Wave (upper row) and spectral intensity (bottom row) from one voice recorder as seen in Audacity, the software we used for annotation. Shown is a recording of a single trill call played on a speaker at various distances. There is a steep fall off between 0.05 m (the approximate distance between the animals’ mouth and the recorder) and 1 m. Beyond 1 m, fall off is less steep. Besides lower intensity, the spectrogram also shows less detail, such as the sinusoidal frequency modulation that is typical of trill calls. B. Animals were video-recorded from overhead. A video frame taken at the onset time of a trill call shows two animals wearing voice recorders marked pink and green. The inter-animal distance is 549 mm. C. Spectrograms of the call from the two voice recorders show a difference in intensity that can be used to infer which animal called. This call is attributed to animal 1 (green). D. A video frame with inter-animal distance 76 mm. E. Spectrograms show higher intensity for animal 2 (pink), to whom the call is attributed.

Fig 3. Vocalization rate per animal.

Plotted for different call types when animals are together in the home cage (black) or separated, i.e. when the partner is out (gray) or when they themselves are out (white). Trill calls were the most common call type. The rate of trill was higher during separation than when animals were together.

Fig 4. Timing of calls relative to calls from partner and other animals.

A. Call rate in relation to calls from the partner and other animals in the room. There is a transient increase in call rate shortly after calls from the partner, but not after calls from other animals. Shaded areas indicate the standard error of mean. B. Results from a subset of 6 animals (3 pairs) with an array of microphones in the room, showing a similar pattern as in A, confirming the result found with wearable recorders alone. C. Trills versus all other call types combined. The peak is absent for other call types, showing that the temporal relation at this latency mainly involves trill calls. D. Trill call rate in relation to calls from the partner when together in the home cage, the partner is out, or the animal him/herself is out. This shows that responsiveness to the partner’s calls is strongest when the animal him/herself is out. E. Peak in call rate 0.4–0.9 s after calls from the partner in males and females. In the Together condition, males had a significantly higher peak call rate than females.

Fig 5

Spectral analysis A Example spectrogram (left) and spectrum (right) of a single trill call. The fundamental frequency F0 is indicated. Trill calls often have multiple harmonics. The fundamental frequency is the first (and lowest) harmonic. B. Population mean spectrograms of trill calls in the 3 conditions. The solid and dashed horizontal lines indicate the mean and median F0. C. F0 for the ‘self-out’ condition minus the ‘together’ condition for each animal.