Impact of predator model presentation paradigms on titi monkey alarm sequences

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

Impact of predator model presentation paradigms on titi monkey alarm sequences

Open access funding provided by University of Zurich. This work received funding from the European Research Council under the European Union’s Seventh Framework Programme (FP7/2007–2013)/ERC grant agreement no. 283871 (PI: KZ), the Swiss National Science Foundation (NCCR Evolving Language, Swiss National Science Foundation Agreement #51NF40_180888) and the University of Neuchâtel.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.Publisher PDFPeer reviewe

Mining noise affects loud call structures and emission patterns of wild black-fronted titi monkeys

Anthropogenic noise pollution is increasing and can constrain acoustic communication in animals. Our aim was to investigate if the acoustic parameters of loud calls and their diurnal pattern in the black-fronted titi monkey (Callicebus nigrifrons) are affected by noise produced by mining activity in a fragment of Atlantic Forest in Brazil. We installed two passive acoustic monitoring devices to record sound 24 h/day, 7 days every 2 months, for a year; one unit was close to an opencast mine and the other 2.5 km away from it. Both sites presented similar habitat structures and were inhabited by groups of black-fronted titi monkeys. We quantified the noise at both sites by measuring the equivalent continuous sound level every 2 months for 1 year and quantified the emission of loud calls by titi monkeys through visual inspection of the recordings. The close site presented higher ambient noise levels than the far site. The quantitative comparison of loud calls of black-fronted titi monkeys between the two sites showed less calling activity in the site close to the mine than in the site further away. Approximately 20 % of the calls detected at the site close to the mine were masked by noise from truck traffic. Loud calls were longer at the site far from the mine and the diurnal patterns of vocal activity differed in the amount of calling as well as in the timing of peak calling activity between the two sites. Our results indicate that mining noise may constrain titi monkeys’ long-distance vocal communication. Loud calls occupy a similar frequency band to mining noise, and an increase in ambient noise may be triggering black-fronted titi monkeys to adjust their long-distance communication patterns to avoid masking of their calls. Given that vocalizations are an important means of social interaction in this species, there are concerns about the impact of mining noise on populations exposed to this human activity

Pairing status and stimulus type predict responses to audio playbacks in female titi monkeys

Some paired primates use complex, coordinated vocal signals to communicate within and between family groups. The information encoded within those signals is not well understood, nor is the intricacy of individuals’ behavioral and physiological responses to these signals. Considering the conspicuous nature of these vocal signals, it is a priority to better understand paired primates’ responses to conspecific calls. Pair-bonded titi monkeys (Plecturocebus cupreus) sing duets comprised of the male and female’s long call. Here, we use a playback study to assess female titi monkeys’ responses to different vocal stimuli based on the subject’s pairing status. Six adult female titi monkeys participated in the study at two timepoints—pre-pairing and post-pairing. At each timepoint, subjects underwent three distinct playbacks—control recording, male solo vocalization, and pair duet. Behaviors such as locomotion and vocalizations were scored during and after the playback, and cortisol and androgen values were assessed via a plasma blood sample. Female titi monkeys attended more to social signals compared to the control, regardless of pairing status. However, in the time immediately following any playback type, female titi monkeys trilled more and spent a greater proportion of time locomoting during pre-pairing timepoints (compared to post-pairing). Female titi monkeys’ behavioral responses to social audio stimuli, combined with subjects’ increases in cortisol and androgens as paired individuals, imply female titi monkeys attend and respond to social signals territorially

Affiliative Behaviors in Pairbonded Red Titi Monkeys (Callicebus Discolor)

Adult titi monkeys (Callicebus spp.) form strong pairbonds and reside in socially monogamous groups. In addition, adult males are heavily involved in infant care, exhibiting a degree of direct investment unusual even among primate species with paternal care. Most of the research exploring the nature of these social bonds has focused on captive populations, and data on wild titi populations are limited. In particular, data quantifying the pairbond and exploring the costs of infant care are rare for wild titi monkeys. I analyzed data from two groups of titi monkeys (Callicebus discolor) in Yasuní National Park and Biosphere Reserve and quantified the affiliative social interactions between the adult male and the adult female in the group to determine 1) the frequency and type of affiliative behaviors exhibited by pairmates, 2) whether there is evidence for sex differences in maintenance of affiliative behaviors and proximity, and 3) whether there is evidence of social costs within a pair during the period when infant care is provided. The most frequent affiliative behaviors involved pairmates resting in close proximity to each other. In addition, males and females spent significantly less time within five meters of each other when they were providing direct infant care, consistent with the prediction that infant care may correlate with a decrease in affiliative behaviors between pairmates. Although no solid conclusions can be drawn from this preliminary study given the small sample size, this research provides data suggesting that the presence of a dependent infant may influence the quality of the relationship between pairmates

The Evolution of Primate Societies - Chapter 3

Compared with other primates, New World monkeys display relatively limited ecological variability. New World monkey anatomy and social systems, however, are extremely diverse. Several unique morphological features (e.g., claws, prehensile tails) and uncommon patterns of social organization (e.g., paternal care, cooperative breeding, female dispersal) have evolved in some platyrrhine species. Social organization and mating patterns include typical harem- like structures where mating is largely polygynous, and large multimale, multifemale groups with promiscuous mating and fi ssion- fusion societies. In addition, some species are socially monogamous and polyandrous. Even closely related species may exhibit strikingly different social organizations, as the example of the squirrel monkeys demonstrates (Mitchell et al. 1991; Boinski et al. 2005b). New World monkey behavior varies within species as well as between them. While the behavior of many species is known from only one study site, intriguing patterns of intraspecific variation are beginning to emerge from observations of populations that sometimes live in close proximity. For example, spider monkeys are often described as showing sex- segregated ranging behavior. Several studies show that males range farther, travel faster, and use larger areas than females, who tend to restrict their habitual ranging to smaller core areas within a group’s large territory (Symington 1988; Chapman 1990; Shimooka 2005). In at least one well- studied population in Yasuní National Park, Ecuador, however, males and females both travel over the entire community home range, and different females within the community show little evidence of occupying distinct core areas (Spehar et al. 2010). Similarly, in most well- studied populations of spider monkeys, females disperse and the resident males within a group are presumed to be close relatives—a suggestion corroborated by genetic data for one local population of spider monkeys in Yasuní. Still, in a different local population, males are not closely related to one another, an unexpected pattern if signifi cant male philopatry were common (Di Fiore 2009; Di Fiore et al. 2009). While the causes of this local variation in group genetic structure are not clear, it may be signifi cant that the groups examined likely had different histories of contact with humans. For longlived animals who occupy relatively small social groups, the loss of even a handful of individuals to hunting, or to any other demographic disturbance, can have a dramatic impact on a group’s genetic structure. Intragroup social relationships, in turn, are likely to be infl uenced by patterns of intragroup relatedness and by the relative availability of social partners of different age or sex class (chapter 21, this volume). Thus, historical and demographic contingencies are likely to create conditions where considerable local, intrapopulation variation in social systems exists. Slight changes in ecological conditions may also contribute to variation in the behavior of individuals living in a single population over time. For example, some authors have hypothesized that howler monkey populations may undergo dramatic fluctuations in size and composition in response to several ecological factors, including resource abundance, parasite and predation pressure, and climate (Milton 1982; Crockett & Eisenberg 1986; Crockett 1996; Milton 1996; Rudran & Fernandez- Duque 2003). This variability, not only among populations, but also within populations across time highlights the need for long- term studies. In sum, our understanding of the behavior of New World monkeys has increased dramatically over the past 25 years. This understanding highlights how their behavior varies within populations over time and among populations or species across space. As our knowledge of platyrrhine behavior continues to unfold and is enriched via additional long- term studies, a central challenge will be to explain how these variations arise. It will be important to entertain adaptive explanations while acknowledging that some differences may emerge via stochastic changes in demography (Struhsaker 2008) or nongenetic, relatively short- term, nonadaptive responses to sudden ecological change

Building Babies - Chapter 16

In contrast to birds, male mammals rarely help to raise the offspring. Of all mammals, only among rodents, carnivores, and primates, males are sometimes intensively engaged in providing infant care (Kleiman and Malcolm 1981). Male caretaking of infants has long been recognized in nonhuman primates (Itani 1959). Given that infant care behavior can have a positive effect on the infant’s development, growth, well-being, or survival, why are male mammals not more frequently involved in “building babies”? We begin the chapter defining a few relevant terms and introducing the theory and hypotheses that have historically addressed the evolution of paternal care. We then review empirical findings on male care among primate taxa, before focusing, in the final section, on our own work on paternal care in South American owl monkeys (Aotus spp.). We conclude the chapter with some suggestions for future studies.Deutsche Forschungsgemeinschaft (HU 1746/2-1) Wenner-Gren Foundation, the L.S.B. Leakey Foundation, the National Geographic Society, the National Science Foundation (BCS-0621020), the University of Pennsylvania Research Foundation, the Zoological Society of San Dieg

Cross-Species Transmission of a Novel Adenovirus Associated with a Fulminant Pneumonia Outbreak in a New World Monkey Colony

Adenoviruses are DNA viruses that naturally infect many vertebrates, including humans and monkeys, and cause a wide range of clinical illnesses in humans. Infection from individual strains has conventionally been thought to be species-specific. Here we applied the Virochip, a pan-viral microarray, to identify a novel adenovirus (TMAdV, titi monkey adenovirus) as the cause of a deadly outbreak in a closed colony of New World monkeys (titi monkeys; Callicebus cupreus) at the California National Primate Research Center (CNPRC). Among 65 titi monkeys housed in a building, 23 (34%) developed upper respiratory symptoms that progressed to fulminant pneumonia and hepatitis, and 19 of 23 monkeys, or 83% of those infected, died or were humanely euthanized. Whole-genome sequencing of TMAdV revealed that this adenovirus is a new species and highly divergent, sharing <57% pairwise nucleotide identity with other adenoviruses. Cultivation of TMAdV was successful in a human A549 lung adenocarcinoma cell line, but not in primary or established monkey kidney cells. At the onset of the outbreak, the researcher in closest contact with the monkeys developed an acute respiratory illness, with symptoms persisting for 4 weeks, and had a convalescent serum sample seropositive for TMAdV. A clinically ill family member, despite having no contact with the CNPRC, also tested positive, and screening of a set of 81 random adult blood donors from the Western United States detected TMAdV-specific neutralizing antibodies in 2 individuals (2/81, or 2.5%). These findings raise the possibility of zoonotic infection by TMAdV and human-to-human transmission of the virus in the population. Given the unusually high case fatality rate from the outbreak (83%), it is unlikely that titi monkeys are the native host species for TMAdV, and the natural reservoir of the virus is still unknown. The discovery of TMAdV, a novel adenovirus with the capacity to infect both monkeys and humans, suggests that adenoviruses should be monitored closely as potential causes of cross-species outbreaks