Marco Gamba

BORIS: a free, versatile open‐source event‐logging software for video/audio coding and live observations

Summary Quantitative aspects of the study of animal and human behaviour are increasingly relevant to test hypotheses and find empirical support for them. At the same time, photo and video cameras can store a large number of video recordings and are often used to monitor the subjects remotely. Researchers frequently face the need to code considerable quantities of video recordings with relatively flexible software, often constrained by species-specific options or exact settings. BORIS is a free, open-source and multiplatform standalone program that allows a user-specific coding environment to be set for a computer-based review of previously recorded videos or live observations. Being open to user-specific settings, the program allows a project-based ethogram to be defined that can then be shared with collaborators, or can be imported or modified. Projects created in BORIS can include a list of observations, and each observation may include one or two videos (e.g. simultaneous screening of visual stimuli and the subject being tested; recordings from different sides of an aquarium). Once the user has set an ethogram, including state or point events or both, coding can be performed using previously assigned keys on the computer keyboard. BORIS allows definition of an unlimited number of events (states/point events) and subjects. Once the coding process is completed, the program can extract a time-budget or single or grouped observations automatically and present an at-a-glance summary of the main behavioural features. The observation data and time-budget analysis can be exported in many common formats (TSV, CSV, ODF, XLS, SQL and JSON). The observed events can be plotted and exported in various graphic formats (SVG, PNG, JPG, TIFF, EPS and PDF).

Quantitative acoustic analysis of the vocal repertoire of the crowned lemur

Only a preliminary qualitative description of the vocal repertoire of Eulemur coronatus is available and no quantitative study of the calls of any wild or captive crowned lemur has ever been performed. The aim of this study was to verify whether the categories of calls in the crowned lemurs vocal repertoire briefly described on qualitatively bases by Macedonia & Stanger (1994) correspond to discrete phonetic categories. Through all-occurrence and focal animal observations, we recorded the vocal activity of 37 crowned lemurs housed in five institutions, both in Europe and Madagascar. We measured both temporal and spectral properties to describe calls quantitatively. We extracted acoustic parameters in the perspective of the source-filter theory of sound production. From spectrograms, we measured call duration and 6 larynx-related features and, using Linear Predictive Coding spectra, we measured four vocal tract related acoustic properties. From a preliminary qualitative inspection of the spectrograms, we identified the 12 types of vocalizations previously described by Macedonia & Stanger (1994) and partially by Petter & Charles-Dominique (1979). Our quantitative analysis has statistical support for a clear classification of 10 acoustic types: Long Grunt, Long Grunt Clear Call, Grunted Hoot, Grunt, Snort, Click, Hoot, Alarm Call, Tonal Call and Scream. In particular, cross-validated Discriminant Function Analysis successfully classified a high percentage of the vocal signals in the 10 vocal categories. Acoustic cues of both larynx-related and vocal tract-related acoustic parameters also offered preliminary support for both sex and individual identity potential that should be more thoroughly investigated in future studies.

Acoustic cues to caller identity in lemurs: a case study

This study investigated the acoustic structure of grunt vocalizations in red-bellied lemurs (Eulemur rubriventer) and its potential for individual discrimination. Acoustic analyses were performed on 1,605 grunts recorded from seven lemurs belonging to two captive groups. From the perspective of sound-filter theory, we described the acoustic structure of grunts, measuring two sets of parameters: fundamental frequency characteristics as larynx-related variables and four formant frequencies as filter-related features. Formants were effective in assigning 80.5% of the vocalizations to the correct emitter against 24.9% scored by the model based on larynx-related variables. We concluded that vocal tract resonances might potentially provide conspecifics with individual cues.

Vocal Tract Morphology Determines Species-Specific Features in Vocal Signals of Lemurs (Eulemur)

The source-filter theory describes vocal production as a two-stage process involving the generation of a sound source, with its own spectral structure, which is then filtered by the resonant properties of the vocal tract. This theory has been successfully applied to the study of animal vocal signals since the 1990s. As an extension, models reproducing vocal tract resonance can be used to reproduce formant patterns and to understand the role of vocal tract filtering in nonhuman vocalizations. We studied three congeneric lemur species —Eulemur fulvus, E. macaco, E. rubriventer— using morphological measurements to build computational models of the vocal tract to estimate formants, and acoustic analysis to measure formants from natural calls. We focused on call types emitted through the nose, without apparent articulation. On the basis of anatomical measurements, we modeled the vocal tract of each species as a series of concatenated tubes, with a cross-sectional area that changed along the tract to approximate the morphology of the larynx, the nasopharyngeal cavity, the nasal chambers, and the nostrils. For each species, we calculated the resonance frequencies in 2500 randomly generated vocal tracts, in which we simulated intraspecific length and size variation. Formant location and spacing showed significant species-specific differences determined by the length of the vocal tract. We then measured formants of a set of nasal vocalizations (“grunts”) recorded from captive lemurs of the same species. We found species-specific differences in the natural calls. This is the first evidence that morphology of the vocal tract is relevant in generating filter-related acoustic cues that potentially provide receivers with information about the species of the emitter.

The use of Artificial Neural Networks to classify primate vocalizations: a pilot study on black lemurs

The identification of the vocal repertoire of a species represents a crucial prerequisite for a correct interpretation of animal behavior. Artificial Neural Networks (ANNs) have been widely used in behavioral sciences, and today are considered a valuable classification tool for reducing the level of subjectivity and allowing replicable results across different studies. However, to date, no studies have applied this tool to nonhuman primate vocalizations. Here, we apply for the first time ANNs, to discriminate the vocal repertoire in a primate species, Eulemur macaco macaco. We designed an automatic procedure to extract both spectral and temporal features from signals, and performed a comparative analysis between a supervised Multilayer Perceptron and two statistical approaches commonly used in primatology (Discriminant Function Analysis and Cluster Analysis), in order to explore pros and cons of these methods in bioacoustic classification. Our results show that ANNs were able to recognize all seven vocal categories previously described (92.5–95.6%) and perform better than either statistical analysis (76.1–88.4%). The results show that ANNs can provide an effective and robust method for automatic classification also in primates, suggesting that neural models can represent a valuable tool to contribute to a better understanding of primate vocal communication. The use of neural networks to identify primate vocalizations and the further development of this approach in studying primate communication are discussed. Am. J. Primatol. 72:337–348, 2010.

Vocal individuality cues in the African penguin (Spheniscus demersus): a source-filter theory approach.

The African penguin is a nesting seabird endemic to southern Africa. In penguins of the genus Spheniscus vocalisations are important for social recognition. However, it is not clear which acoustic features of calls can encode individual identity information. We recorded contact calls and ecstatic display songs of 12 adult birds from a captive colony. For each vocalisation, we measured 31 spectral and temporal acoustic parameters related to both source and filter components of calls. For each parameter, we calculated the Potential of Individual Coding (PIC). The acoustic parameters showing PIC ≥ 1.1 were used to perform a stepwise cross-validated discriminant function analysis (DFA). The DFA correctly classified 66.1% of the contact calls and 62.5% of display songs to the correct individual. The DFA also resulted in the further selection of 10 acoustic features for contact calls and 9 for display songs that were important for vocal individuality. Our results suggest that studying the anatomical constraints that influence nesting penguin vocalisations from a source-filter perspective, can lead to a much better understanding of the acoustic cues of individuality contained in their calls. This approach could be further extended to study and understand vocal communication in other bird species.

Interspecific semantic alarm call recognition in the solitary Sahamalaza sportive lemur, Lepilemur sahamalazensis.

As alarm calls indicate the presence of predators, the correct interpretation of alarm calls, including those of other species, is essential for predator avoidance. Conversely, communication calls of other species might indicate the perceived absence of a predator and hence allow a reduction in vigilance. This “eavesdropping” was demonstrated in birds and mammals, including lemur species. Interspecific communication between taxonomic groups has so far been reported in some reptiles and mammals, including three primate species. So far, neither semantic nor interspecific communication has been tested in a solitary and nocturnal lemur species. The aim of this study was to investigate if the nocturnal and solitary Sahamalaza sportive lemur, Lepilemur sahamalazensis, is able to access semantic information of sympatric species. During the day, this species faces the risk of falling prey to aerial and terrestrial predators and therefore shows high levels of vigilance. We presented alarm calls of the crested coua, the Madagascar magpie-robin and aerial, terrestrial and agitation alarm calls of the blue-eyed black lemur to 19 individual Sahamalaza sportive lemurs resting in tree holes. Songs of both bird species’ and contact calls of the blue-eyed black lemur were used as a control. After alarm calls of crested coua, Madagascar magpie-robin and aerial alarm of the blue-eyed black lemur, the lemurs scanned up and their vigilance increased significantly. After presentation of terrestrial alarm and agitation calls of the blue-eyed black lemur, the animals did not show significant changes in scanning direction or in the duration of vigilance. Sportive lemur vigilance decreased after playbacks of songs of the bird species and contact calls of blue-eyed black lemurs. Our results indicate that the Sahamalaza sportive lemur is capable of using information on predator presence as well as predator type of different sympatric species, using their referential signals to detect predators early, and that the lemurs’ reactions are based on experience and learning.

Behavioral correlates of extra-pair copulation in Indri indri

Active pursuit of extra-pair mating has been reported for Indri indri, the socially monogamous largest living lemur. This study, conducted in a mountain rainforest in eastern Madagascar, presents the first evidence for extra-pair mating of indri and discusses the alternative mating strategy and alteration of the social, territorial, spatial, and vocal behavior of the adult female of a group of wild indris. Further studies may investigate whether extra-pair copulation is an attempt to breed with a partner of superior quality and thus lead to extra-pair paternity. If so, it could potentially play a role in maintaining genetic variability within a population.

The songs of the indris (Mammalia: Primates: Indridae): contextual variation in the long-distance calls of a lemur

Abstract Contextual variation in the loud calls of strepsirhine primates is poorly understood. To understand whether songs given by indris in different contexts represent acoustically distinct variants and have the potential to elicit context-specific behaviours in conspecific listeners, we investigated the acoustic variability of these songs and the distance travelled by vocalizers after their emissions. Songs of 41 individuals were recorded from 16 indri groups in four different forest sites in eastern Madagascar. We collected a total of 270 duets and choruses arising during territorial defence, advertisement and cohesion. We demonstrated that the structure of indri songs conveyed context-specific information through their overall duration, but shared the sequential pattern of harsh units (roars) followed by long notes and, finally, descending phrases. Analysing in detail individual contributions to advertisement songs and cohesion songs, we found that the acoustic structure of units could be classified correctly with a high degree of reliability (96.23% of long notes, 80.16% of the descending phrases, 72.54% of roars). Future investigations using playback stimuli could explore the relationship between acoustic features and the information transmitted by the song.

Comparative Analysis of the Vocal Repertoire of Eulemur : A Dynamic Time Warping Approach

The diversity of qualitative approaches and analytical methods has often undermined comparative research on primate vocal repertoires. The purpose of the present work is to introduce a quantitative method based on dynamic time warping to the study of repertoire size in Eulemur spp. We obtained a large sample of calls of E. coronatus, E. flavifrons, E. fulvus, E. macaco, E. mongoz, E. rubriventer, and E. rufus, recorded between 1999 and 2013 from captive and wild lemurs. We inspected recordings visually using spectrograms, then cut and saved high-quality vocal emissions to single files for further analysis. We extracted the acoustic features of all vocalizations of a species using the Hidden Markov Model Toolkit, an application of dynamic time warping, and then compared cepstral coefficients (a feature widely used in automatic speaker recognition) pairwise. We analyzed the results using affinity propagation clustering. We found that Eulemur species share most of their vocal repertoire but species-specific calls determine repertoire size differences. Repertoire size varied from 9 to 14 vocalization types among species, with a mean of 11.