02307nas a2200241 4500008004100000022001400041245009600055210006900151260001600220490000700236520154300243653002201786653001901808653002201827653002401849653001901873100002601892700002501918700002601943700002401969700001701993856005502010 2018 eng d a0340-544300aAge and social affinity effects on contact call interactions in free-ranging spider monkeys0 aAge and social affinity effects on contact call interactions in  cJan-12-20180 v723 a

Nonhuman primates’ vocal repertoire has shown little plasticity, with immatures producing adult-like acoustic structures. Yet, the use of different call types shows a degree of socially dependent flexibility during development. In several nonhuman primate species, group members exchange contact calls respecting a set of social and temporal rules that may be learned (e.g., overlap avoidance, turn-taking, social selection of interacting partners, and call type matching). Here, we study the use of contact calls in free-living adult and immature (old and young) spider monkeys (Ateles geoffroyi). We focused our study in two contact call types of the species’ repertoire: whinnies and high-whinnies. Our results suggest that individuals in all age classes produced both call types, with immatures producing less frequently the whinny call type. Immature individuals exchanged calls less often than adults, although their contribution increased with age. Conversely, mature individuals regulated their emissions by (1) exchanging more calls with their preferred affiliative partner and (2) matching the call type, while immatures did not. Our results show that contact call usage changes during development and suggest that adult rules might be learned. We argue that call matching is a “conversational rule” that young individuals acquire with apparent call-type-dependent variations during development. Our findings support the idea that social factors influence vocal development in nonhuman primates.

10aAcoustic matching10aCall exchanges10aNew World monkeys10avocal communication10avocal learning1 aBriseno-Jaramillo, M.1 aRamos-Fernández, G.1 aPalacios-Romo, T., M.1 aSosa-López, J., R.1 aLemasson, A. uhttp://link.springer.com/10.1007/s00265-018-2615-202743nas a2200253 4500008004100000022001300041245008900054210006900143260001600212300001400228490000800242520177400250653001502024653003202039653002902071653002902100653001302129653002402142653002902166653001902195100002002214700002202234856023302256 2018 eng d a0003347200aExperimental evidence that titi and saki monkey alarm calls deter an ambush predator0 aExperimental evidence that titi and saki monkey alarm calls dete cJan-11-2018 a141 - 1470 v1453 a

Many animals use alarm calls in intraspecific communication to warn conspecifics of a predator's presence or to elicit coordinated group responses. However, alarm calls may also be aimed directly at the predator to discourage further pursuit. These 'pursuit-deterrent' signals are particularly important in the presence of ambush predators that rely on stealth to hunt prey. Here, we conducted playback experiments over a 16-month period on radiocollared ocelots, Leopardus pardalis, in Peru using audio stimuli of titi monkey (Callicebus toppini) and saki monkey (Pithecia rylandsi) alarm calls, with nonalarm loud calls as controls. We predicted that, if titi and saki alarm calls function as deterrent signals, then ocelots would move away from the sound source and leave the area following exposure to alarms but not following controls. We tracked ocelots via radiotelemetry for 30 min prior to and 30 min following experiments. At 15 min intervals we noted subject location, whether the cat was stationary or moving towards, away from or parallel to the playback area (calculated using a deflection angle) and distance travelled. Results showed a significantly different pattern in response movement between playback trials; ocelots moved away from the sound source in the majority of alarm trials but remained stationary/hidden or moved in a variety of directions following control trials. Ocelots also moved significantly farther following exposure to alarm trials than following exposure to controls. We conclude that ocelots can distinguish alarm calls from other loud calls and are deterred by alarm-calling monkeys. This is the first study to use playbacks on wild predators to test the pursuit-deterrent function of primate alarm calls.

10aCallicebus10ainterspecific communication10aLeopardus pardalisocelot10aperception advertisement10aPithecia10aplayback experiment10apursuit-deterrent signal10aradiotelemetry1 aAdams, Dara, B.1 aKitchen, Dawn, M. uhttps://linkinghub.elsevier.com/retrieve/pii/S000334721830280Xhttps://api.elsevier.com/content/article/PII:S000334721830280X?httpAccept=text/xmlhttps://api.elsevier.com/content/article/PII:S000334721830280X?httpAccept=text/plain01982nas a2200157 4500008004100000022001400041245010800055210006900163260001600232300001600248490000800264520146300272100002001735700001801755856005101773 2018 eng d a0001-496600aFrom behavior to physiology and back again: The role of auditory cortex in vocal production and control0 aFrom behavior to physiology and back again The role of auditory  cJan-09-2018 a1898 - 18990 v1443 a

Vocal communication plays an important role in the lives of both humans and many animal species. Ensuring accurate communication, however, requires auditory self-monitoring to control vocal production and rapidly compensate for errors in vocal output. Despite the importance of this process, the underlying neural mechanisms are relatively unknown. Previous work has demonstrated that neurons in the auditory cortex are suppressed during vocal production, while simultaneously maintaining their sensitivity to vocal feedback, suggesting a role in auditory self-monitoring. The behavioral role of auditory cortex in vocal control, however, remains unclear. We investigated the function of auditory cortical activity during vocal self-monitoring and feedback-dependant vocal control in marmoset monkeys. Using real-time frequency-shifted feedback during vocalization, we demonstrate that marmosets exhibit rapid compensatory changes in vocal production, a feedback-dependent behavior that is predicted by the activities of neurons in auditory cortex. We further establish the role of auditory cortex in vocal control using electrical microstimulation to evoke rapid changes in produced vocalizations. These findings suggest a causal role for the auditory cortex in vocal self-monitoring and feedback-dependent vocal control, linking mechanisms of production and perception, and have important implications for understanding human speech motor control.

1 aEliades, Steven1 aTsunada, Joji uhttp://asa.scitation.org/doi/10.1121/1.506831701942nas a2200157 4500008004100000022001400041245012000055210006900175260001600244300001600260490000800276520139900284100002101683700002901704856005101733 2018 eng d a0001-496600aNeuronal frequency selectivity in the inferior colliculus and cochlear nucleus of the awake behaving macaque monkey0 aNeuronal frequency selectivity in the inferior colliculus and co cJan-09-2018 a1935 - 19350 v1443 a

Frequency selectivity relates to the ability to process complex signals and can be measured through auditory filters. Behavioral filters show broader tuning compared to cochlear and auditory nerve fiber tuning. To test whether filters evolve across the auditory pathway or if they are established in the periphery, we estimated neural filters in the cochlear nucleus (CN) and inferior colliculus (IC) and compared with simultaneously measured behavioral filters in macaques. Three macaques were trained to detect tones (signal = unit characteristic frequency (CF)) in spectrally notched maskers of varying width while single unit responses were recorded in the CN and IC. Filter shapes and bandwidths were estimated from the masked thresholds using the rounded exponential fit. Behavioral and neural filters increased in bandwidth with increasing CF. Behavioral and neural bandwidths were significantly correlated and not significantly different from each other for the CN and IC. Neural filter bandwidths were variable across units and structures, possibly reflecting heterogeneity of neuronal encoding strategies. These findings support a model in which behavioral frequency selectivity is established early in the auditory pathway. These data form the baseline for ongoing studies of macaques with noise-induced hearing loss and future studies of emerging hearing loss therapeutics.

1 aBurton, Jane, A.1 aRamachandran, Ramnarayan uhttp://asa.scitation.org/doi/10.1121/1.506846602567nas a2200205 4500008004100000022001300041245008200054210006900136260001600205520171200221653002301933653002501956653003501981653001302016653002802029653002702057100002202084700002202106856023302128 2018 eng d a0165027000aSemi-chronic laminar recordings in the brainstem of behaving marmoset monkeys0 aSemichronic laminar recordings in the brainstem of behaving marm cJan-10-20183 a

Background

Chronic recordings with multi-electrode arrays are widely used to study neural networks underlying complex primate behaviors. Most of these systems are designed for studying neural activity in the cortical hemispheres resulting in a lack of devices being capable of simultaneously recording from ensembles of neurons in deep brainstem structures. However, to fully understand complex behavior, it is fundamental to also decipher the intrinsic mechanisms of the underlying motor pattern generating circuits in the brainstem.

New Method

We report a light-weight system that simultaneously measures single-unit activity from a large number of recording sites in the brainstem of marmoset monkeys. It includes a base chamber fixed to the animal’s skull and a removable upper chamber that can be semi-chronically mounted to the base chamber to flexibly position an embedded micro-drive containing a 32-channel laminar probe to record from various positions within the brainstem for several weeks.

Results

The current system is capable of simultaneously recording stable single-unit activity from a large number of recording sites in the brainstem of vocalizing marmoset monkeys.

Comparison with Existing Methods

To the best of our knowledge, chronic systems to record from deep brainstem structures with multi-site laminar probes in awake, behaving monkeys do not yet exist.

Conclusions

The semi-chronic implantation of laminar electrodes into the brainstem of behaving marmoset monkeys opens new research possibilities in fully understanding the neural mechanisms underlying complex behaviors in marmoset monkeys.

10aCallithrix jacchus10aimplanted electrodes10alaminar multi-site microprobes10aprimates10asemi-chronic recordings10asingle-unit recordings1 aPomberger, Thomas1 aHage, Steffen, R. uhttps://linkinghub.elsevier.com/retrieve/pii/S0165027018303406https://api.elsevier.com/content/article/PII:S0165027018303406?httpAccept=text/xmlhttps://api.elsevier.com/content/article/PII:S0165027018303406?httpAccept=text/plain03063nas a2200229 4500008004100000022001300041245012100054210006900175260001600244520211700260653002502377653001602402653003002418653001202448653001802460100002202478700002302500700002002523700003702543700002002580856023302600 2018 eng d a0168159100aDomestic piglets (Sus scrofa domestica) are attentive to human voice and able to discriminate some prosodic features0 aDomestic piglets Sus scrofa domestica are attentive to human voi cJan-10-20183 a

Vocal communication is of major social importance in pigs. Their auditory sensitivity goes beyond the intraspecific level; studies have shown that domestic pigs are sensitive to and can learn to recognise human voices. The question of which prosodic features (intonation, accentuation, rhythm) of human speech may matter to this recognition, however, remains open. A total of 42 piglets were allocated to three experimental groups. Each piglet was submitted to three choice tests, during which different pairs of sounds were broadcast. Each group was first offered a choice between an unmodified (neutral) human voice and a background noise, in order to verify the attractiveness of human voice. We found that piglets could distinguish human voice; they gazed more rapidly (P < 0.05) and for longer (P < 0.05) in the direction of the human voice than in the direction of the background noise. Group 1 was then submitted to artificially modified voices: low vs high-pitched, and then slow vs rapid rhythm. Group 2 was submitted to artificially modified voices with a combination of these features: rapid and high-pitched vs slow and low-pitched, and then slow and high-pitched vs rapid and low-pitched. Group 3 was submitted to naturally recorded voices coding for different emotions (happiness vs anger) and then different intonations (interrogation vs command). We found that piglets approached the loudspeaker broadcasting the rapid rhythm (6 s (2–32)) more rapidly than the loudspeaker broadcasting the slow rhythm (33 s (15–70); p < 0.05). They also spent more time near the loudspeaker broadcasting the “high-pitched and slow” voice (86 s (52–110)) than near the one broadcasting the “low-pitched and rapid” voice (29 s (9–73); W = 86, P < 0.05). In sum, the sensitivity of piglets for human prosody was moderate but not inexistent. Our results suggest that piglets base their responses to human voice on a combination of prosodic features.

10aAuditory preferences10aChoice test10aHuman-animal relationship10aPiglets10aVoice prosody1 aBensoussan, Sandy1 aTigeot, Raphaëlle1 aLemasson, Alban1 aMeunier-Salaün, Marie-Christine1 aTallet, Céline uhttps://linkinghub.elsevier.com/retrieve/pii/S0168159118301485https://api.elsevier.com/content/article/PII:S0168159118301485?httpAccept=text/xmlhttps://api.elsevier.com/content/article/PII:S0168159118301485?httpAccept=text/plain02071nas a2200205 4500008004100000022001400041245010800055210006900163260001600232520140100248653001201649653001101661653001601672653001701688100001801705700002101723700001901744700002401763856007801787 2018 eng d a1674-550700aTemporal adjustment of short calls according to a partner during vocal turn-taking in Japanese macaques0 aTemporal adjustment of short calls according to a partner during cMar-10-20193 a

Turn-taking is a common feature in human speech, and is also seen in the communication of other primate species. However, evidence of turn-taking in vocal exchanges within a short time frame is still scarce in nonhuman primates. This study investigated whether dynamic adjustment during turn-taking in short calls exists in Japanese macaques Macaca fuscata. We observed exchanges of short calls such as grunts, girneys, and short, low coos during social interactions in a free-ranging group of Japanese macaques. We found that the median gap between the turns of two callers was 250 ms. Call intervals varied among individuals, suggesting that call intervals were not fixed among individuals. Solo call intervals were shorter than call intervals interrupted by responses from partners (i.e., exchanges) and longer than those between the partner’s reply and the reply to that call, indicating that the monkeys did not just repeat calls at certain intervals irrespective of the social situation. The differences in call intervals during exchanged and solo call sequences were explained by the response interval of the partner, suggesting an adjustment of call timing according to the tempo of the partner’s call utterance. These findings suggest that monkeys display dynamic temporal adjustment in a short time window, which is comparable to turn-taking in human speech.

10aprimate10arhythm10aturn-taking10avocalization1 aKatsu, Noriko1 aYamada, Kazunori1 aOkanoya, Kazuo1 aNakamichi, Masayuki uhttps://academic.oup.com/cz/advance-article/doi/10.1093/cz/zoy077/513269002834nas a2200325 4500008004100000245010900041210006900150260001600219300000800235490000600243520186600249653001502115653001502130653001702145653001802162653001302180653002402193100001902217700002202236700002302258700001702281700002102298700002502319700002102344700002902365700002002394700002902414700002202443856004302465 2018 eng d00aDuetting Patterns of Titi Monkeys (Primates, Pitheciidae: Callicebinae) and Relationships with Phylogeny0 aDuetting Patterns of Titi Monkeys Primates Pitheciidae Callicebi cJan-10-2018 a1780 v83 a

Long-range vocal communication in socially monogamous titi monkeys is mediated by the production of loud, advertising calls in the form of solos, duets, and choruses. We conducted a power spectral analysis of duets and choruses (simply “duets” hereafter) followed by linear discriminant analysis using three acoustic parameters—dominant frequency of the combined signal, duet sequence duration, and pant call rate—comparing the coordinated vocalizations recorded from 36 family groups at 18 sites in Bolivia, Peru and Ecuador. Our analysis identified four distinct duetting patterns: (1) a donacophilus pattern, sensu stricto, characteristic of P. donacophilus, P. pallescens, P. olallae, and P. modestus; (2) a moloch pattern comprising P. discolor, P. toppini, P. aureipalatii, and P. urubambensis; (3) a torquatus pattern exemplified by the duet of Cheracebus lucifer; and (4) the distinctive duet of P. oenanthe, a putative member of the donacophilus group, which is characterized by a mix of broadband and narrowband syllables, many of which are unique to this species. We also document a sex-related difference in the bellow-pant phrase combination among the three taxa sampled from the moloch lineage. Our data reveal a presumptive taxonomic incoherence illustrated by the distinctive loud calls of both P. urubambensis and P. oenanthe within the donacophilus lineage, sensu largo. The results are discussed in light of recent reassessments of the callicebine phylogeny, based on a suite of genetic studies, and the potential contribution of environmental influences, including habitat acoustics and social learning. A better knowledge of callicebine loud calls may also impact the conservation of critically endangered populations, such as the vocally distinctive Peruvian endemic, the San Martin titi, P. oenanthe.

10aCallicebus10aCheracebus10aconservation10aPlecturocebus10ataxonomy10avocal communication1 aAdret, Patrice1 aDingess, Kimberly1 aCaselli, Christini1 aVermeer, Jan1 aMartínez, Jesus1 aAmancio, Jossy, Luna1 avan Kuijk, Silvy1 aLineros, Lucero, Hernani1 aWallace, Robert1 aFernandez-Duque, Eduardo1 aDi Fiore, Anthony uhttp://www.mdpi.com/2076-2615/8/10/17802456nas a2200229 4500008004100000245010700041210006900148260001600217300001300233490000700246520173400253100001901987700001902006700002402025700001902049700002702068700002402095700002202119700001702141700001602158856005202174 2018 eng d00aCall and be counted! Can we reliably estimate the number of callers in the indri's (Indri indri) song?0 aCall and be counted Can we reliably estimate the number of calle cMar-08-2018 ae02016640 v133 a

Estimating the number of animals participating in a choral display may contribute reliable information on animal population estimates, particularly when environmental or behavioral factors restrict the possibility of visual surveys. Difficulties in providing a reliable estimate of the number of singers in a chorus are many (e.g., background noise masking, overlap). In this work, we contributed data on the vocal chorusing of the indri lemurs (Indri indri), which emit howling cries, known as songs, uttered by two to five individuals. We examined whether we could estimate the number of emitters in a chorus by screening the fundamental frequency in the spectrograms and the total duration of the songs, and the reliability of those methods when compared to the real chorus size. The spectrographic investigation appears to provide reliable information on the number of animals participating in the chorusing only when this number is limited to two or three singers. We also found that the Acoustic Complexity Index positively correlated with the real chorus size, showing that an automated analysis of the chorus may provide information about the number of singers. We can state that song duration shows a correlation with the number of emitters but also shows a remarkable variation that remains unexplained. The accuracy of the estimates can reflect the high variability in chorus size, which could be affected by group composition, season and context. In future research, a greater focus on analyzing frequency change occurring during these collective vocal displays should improve our ability to detect individuals and allow a finer tuning of the acoustic methods that may serve for monitoring chorusing mammals.

1 aTorti, Valeria1 aValente, Daria1 aDe Gregorio, Chiara1 aComazzi, Carlo1 aMiaretsoa, Longondraza1 aRatsimbazafy, Jonah1 aGiacoma, Cristina1 aGamba, Marco1 aReby, David uhttp://dx.plos.org/10.1371/journal.pone.020166401928nas a2200169 4500008004100000022001400041245009100055210006900146260001600215300001400231490000800245520138700253100002301640700002101663700002301684856005101707 2018 eng d a0001-496600aClassification of producer characteristics in primate long calls using neural networks0 aClassification of producer characteristics in primate long calls cJan-07-2018 a344 - 3530 v1443 a

Primate long calls are high-amplitude vocalizations that can be critical in maintaining intragroup contact and intergroup spacing, and can encode abundant information about a call's producer, such as age, sex, and individual identity. Long calls of the wild emperor (Saguinus imperator) and saddleback (Leontocebus weddelli) tamarins were tested for these identity signals using artificial neural networks, machine-learning models that reduce subjectivity in vocalization classification. To assess whether modelling could be streamlined by using only factors which were responsible for the majority of variation within networks, each series of networks was re-trained after implementing two methods of feature selection. First, networks were trained and run using only the subset of variables whose weights accounted for ≥50% of each original network's variation, as identified by the networks themselves. In the second, only variables implemented by decision trees in predicting outcomes were used. Networks predicted dependent variables above chance (≥58.7% for sex, ≥69.2 for age class, and ≥38.8% for seven to eight individuals), but classification accuracy was not markedly improved by feature selection. Findings are discussed with regard to implications for future studies on identity signaling in vocalizations and streamlining of data analysis.

1 aRobakis, Efstathia1 aWatsa, Mrinalini1 aErkenswick, Gideon uhttp://asa.scitation.org/doi/10.1121/1.504652602806nas a2200181 4500008004100000245013700041210006900178260001600247300001400263490000800277520219800285653001402483653001402497653003202511653001702543100001902560856004502579 2018 eng d00aTemporal patterns of chimpanzee loud calls in the Issa Valley, Tanzania: Evidence of nocturnal acoustic behavior in wild chimpanzees0 aTemporal patterns of chimpanzee loud calls in the Issa Valley Ta cJan-07-2018 a530 - 5400 v1663 a

Objectives: Much is known about chimpanzee diurnal call patterns, but far less about night-time vocal behavior. I deployed a passive acoustic monitoring (PAM) system to assess 24-hr temporal acoustic activity of wild, unhabituated chimpanzees that live in a woodland mosaic habitat similar to hominin landscapes from the Plio-Pleistocene. A primary aim was to apply findings to our broader understanding to chimpanzee 24-hr activity patterns, and what implications this may have for reconstructing hominin adaptations to similarly hot, dry, and open landscapes. I also tested whether chimpanzees conform to the acoustic adaptation hypothesis, and produce loud calls dur- ing periods of optimal sound transmission.


Methods: Nine custom-made solar-powered acoustic transmission units (SPATUs) recorded con- tinuously for 250 days over 11 months in the Issa Valley, western Tanzania. I complemented acoustic data with environmental data from weather stations as well as behavioral data collected on chimpanzee nest group sizes to assess the relationship between party size and calling.


Results: Chimpanzees called at all hours of the day and night in both wet and dry seasons, and night and day calls exhibited parallel rates/month, although twilight calls were produced signifi- cantly more in the dry, compared to the wet season. Calls were more likely during warmer temperatures and lower humidity. Call rate was positively associated with (nest) party size and counter-calls exhibited no temporal variation in their origins (similar vs. adjacent valleys).


Conclusions: Chimpanzees were acoustically active throughout the 24-hr cycle, although at low rates compared to diurnal activity, revealing night-time activity in an ape otherwise described as diurnal. Chimpanzee loud calls partially, and weakly, conformed to the acoustic adaptation hypoth- esis and likely responded to social, rather than environmental factors. Call rates accurately reflect grouping patterns and PAM is demonstrated to be an effective means of remotely assessing activ- ity, especially at times and from places that are difficult to access for researchers.

10agreat ape10apant hoot10apassive acoustic monitoring10avocalization1 aPiel, Alex, K. uhttp://doi.wiley.com/10.1002/ajpa.v166.3