Impact of predator model presentation paradigms on titi monkey alarm sequences.

Abstract: Predator presentation experiments are widely used to investigate animal alarm vocalizations. They usually involve presentations of predator models or playbacks of predator calls, but it remains unclear whether the two paradigms provide similar results, a major limitation when investigating animal syntactic and semantic capacities. Here, we investigate whether visual and acoustic predator cues elicit different vocal reactions in black-fronted titi monkeys (Callicebus nigrifrons). We exposed six groups of wild titi monkeys to visual models or playbacks of vocalizations of raptor or felid. We characterized each group's vocal reactions using sequence parameters known to reliably encode predatory events in this species. We found that titi monkeys' vocal reactions varied with the predator species but also with the experimental paradigm: while vocal reactions to raptor vocalizations and models were similar, felid vocalizations elicited heterogeneous, different reactions from that given to felid models. We argue that subjects are not familiar with felid vocalizations, because of a lack of learning opportunities due to the silent behaviour of felids. We discuss the implication of these findings for the semantic capacities of titi monkeys. We finally recommend that playbacks of predator vocalizations should not be used in isolation but in combination with visual model presentations, to allow fine-grained analyses of the communication system of prey species. Significance statement: It is common to present prey species with predator models or predator calls to study their vocal reactions. The two paradigms are often used independently, but it remains unclear whether they provide similar results. Here, we studied the vocal reactions of titi monkeys to calls and models of raptors and felids. We show that titi monkeys seem to recognize the vocalizations of raptors but not those of felids. The study of the vocal reactions emitted when titi monkeys cannot clearly identify the threat allows us to draw accurate hypotheses about the meaning of titi monkeys' alarm utterances. We argue that playbacks of predator calls should be used in conjunction with model presentations, which can allow us to better investigate the information and the structure of the alarm systems. Supplementary Information: The online version contains supplementary material available at 10.1007/s00265-022-03250-1.

Dramatic decline in a titi monkey population after the 2016-2018 sylvatic yellow fever outbreak in Brazil.

Platyrrhini are highly vulnerable to the yellow fever (YF) virus. From 2016 to 2018, the Atlantic Forest of southeast Brazil faced its worst sylvatic YF outbreak in about a century, thought to have killed thousands of primates. It is essential to assess the impact of this epidemic on threatened primate assemblages to design effective conservation strategies. In this study, we assessed the impact of the 2016-2018 YF outbreak on a geographically isolated population of Near Threatened black-fronted titi monkeys (Callicebus nigrifrons) in two Atlantic Forest patches of the Santuário do Caraça, MG, Brazil. Extensive preoutbreak monitoring, conducted between 2008 and 2016, revealed that the home range and group sizes of the population remained stable. In 2016, the population size was estimated at 53-57 individuals in 11-12 groups. We conducted monitoring and playback surveys in 2019 and found that the population had decreased by 68% in one forest patch and completely vanished in the other, resulting in a combined decline of 80%. We discuss this severe loss of a previously stable population and conclude that it was highly likely caused by the YF outbreak. The remaining population is at risk of disappearing completely because of its small size and geographic isolation. A systematic population surveys of C. nigrifrons, along other sensible Platyrrhini species, is needed to re-evaluate their current conservation status.

Titi monkeys combine alarm calls to create probabilistic meaning.

Previous work suggested that titi monkeys Callicebus nigrifrons combine two alarm calls, the A- and B-calls, to communicate about predator type and location. To explore how listeners process these sequences, we recorded alarm call sequences of six free-ranging groups exposed to terrestrial and aerial predator models, placed on the ground or in the canopy, and used multimodel inference to assess the information encoded in the sequences. We then carried out playback experiments to identify the features used by listeners to react to the available information. Results indicated that information about predator type and location were encoded by the proportion of B-call pairs relative to all call pairs of the sequence (i.e., proportion of BB-grams). The results suggest that the meaning of the sequence is not conveyed in a categorical but probabilistic manner. We discuss the implications of these findings for current theories of animal communication and language evolution.

Classification and automatic transcription of primate calls.

This paper reports on an automated and openly available tool for automatic acoustic analysis and transcription of primate calls, which takes raw field recordings and outputs call labels time-aligned with the audio. The system's output predicts a majority of the start times of calls accurately within 200 milliseconds. The tools do not require any manual acoustic analysis or selection of spectral features by the researcher.

Acoustic sequences in non-human animals: a tutorial review and prospectus.

Animal acoustic communication often takes the form of complex sequences, made up of multiple distinct acoustic units. Apart from the well-known example of birdsong, other animals such as insects, amphibians, and mammals (including bats, rodents, primates, and cetaceans) also generate complex acoustic sequences. Occasionally, such as with birdsong, the adaptive role of these sequences seems clear (e.g. mate attraction and territorial defence). More often however, researchers have only begun to characterise - let alone understand - the significance and meaning of acoustic sequences. Hypotheses abound, but there is little agreement as to how sequences should be defined and analysed. Our review aims to outline suitable methods for testing these hypotheses, and to describe the major limitations to our current and near-future knowledge on questions of acoustic sequences. This review and prospectus is the result of a collaborative effort between 43 scientists from the fields of animal behaviour, ecology and evolution, signal processing, machine learning, quantitative linguistics, and information theory, who gathered for a 2013 workshop entitled, 'Analysing vocal sequences in animals'. Our goal is to present not just a review of the state of the art, but to propose a methodological framework that summarises what we suggest are the best practices for research in this field, across taxa and across disciplines. We also provide a tutorial-style introduction to some of the most promising algorithmic approaches for analysing sequences. We divide our review into three sections: identifying the distinct units of an acoustic sequence, describing the different ways that information can be contained within a sequence, and analysing the structure of that sequence. Each of these sections is further subdivided to address the key questions and approaches in that area. We propose a uniform, systematic, and comprehensive approach to studying sequences, with the goal of clarifying research terms used in different fields, and facilitating collaboration and comparative studies. Allowing greater interdisciplinary collaboration will facilitate the investigation of many important questions in the evolution of communication and sociality.

Titi monkey call sequences vary with predator location and type.

Animal alarm calls can encode information about a predator's category, size, distance or threat level. In non-human primates, alarm calls typically refer to broad classes of disturbances, in some instances to specific predators. Here, we present the results of a field experiment with a New World primate, the black-fronted titi monkey (Callicebus nigrifrons), designed to explore the information conveyed by their alarm call system. Adults produced sequences consisting of two main alarm call types that conveyed, in different parts of the utterance, information about a predator's type and location. In particular, sequence compositions differed depending on whether the predator was a mammalian carnivore or a raptor, and whether it was detected in a tree or on the ground. This is the first demonstration of a sequence-based alarm call system in a non-human animal that has the capacity to encode both location and type of predatory threat.

Observed case of maternal infanticide in a wild group of black-fronted titi monkeys (Callicebus nigrifrons).

A maternal infanticide was observed in a group of unprovisioned wild black-fronted titi monkeys (Callicebus nigrifrons). An approximately 3-day-old male infant was killed by his mother. A post-mortem revealed the infant to be clinically healthy. We considered various hypotheses to explain why this behavior occurred (e.g., reproductive advantage, stress, nutritional, infant viability and population density). It is noteworthy that the mother and not the father killed the infant, since in this species the father provides considerable infant care from a few hours after birth.

A case of adoption in a wild group of black-fronted titi monkeys (Callicebus nigrifrons).

We observed a case of infant adoption in an unprovisioned group of wild black-fronted titi monkeys (Callicebus nigrifrons). During our long-term field study we noticed that an infant had moved from one of our study groups ("Desbotado") to another ("Rio"). Observations of the adoptive group confirm that it was being cared for by the adult male, and initially the group's adult female was nursing the infant alongside her biological infant. Interestingly, the native and adoptive groups have frequent inter-group interactions, but at no point have we observed the native group trying to retrieve its infant. As of April 2007 the infant has been living in its adoptive group for 19 months. These data document the first case of adoption in this genus; they suggest that infant recognition is poorly developed in this species and that under certain circumstances wild groups of C. nigrifrons can successfully rear twins. In our study population reproductive females give birth to one infant every year; the only case when this has not happened is with the group that adopted the infant, suggesting that adoption may generate a reproductive cost.