Feed-forward inhibition fine-tunes response timing in auditory-vocal interactions

The ability to regulate vocal timing is a fundamental aspect of communicative interactions for many species, including conversational speech among humans, yet little is known about the neural circuitry that regulates the input-dependent timing of vocal replies. Exploring this topic in the zebra finch premotor area HVC, we identify feed-forward inhibition as a key regulator of vocal response timing. Based on a spiking network model informed by behavioral and electrophysiological data from communicating zebra finches, we predicted that two different patterns of inhibition regulate vocal-motor responses. In one scenario, the strength of production-related premotor inhibition translates into plasticity in vocal response delays. In the other scenario, fast transient interneuron activity in response to auditory input results in the suppression of call production while a call is heard, thereby reducing acoustic overlap between callers. Extracellular recordings in HVC during the listening phase confirm the presence of auditory-evoked response patterns in putative inhibitory interneurons, along with corresponding signatures of auditory-evoked activity suppression. The proposed model provides a parsimonious framework to explain how auditory-vocal transformations can give rise to vocal turn-taking and highlights multiple roles of local inhibition for behavioral modulation at different time scales.

Evidence of stereotyped contact call use in narwhal (Monodon monoceros) mother-calf communication

Narwhals (Monodon monoceros) are gregarious toothed whales that strictly reside in the high Arctic. They produce a broad range of signal types; however, studies of narwhal vocalizations have been mostly descriptive of the sounds available in the species’ overall repertoire. Little is known regarding the functions of highly stereotyped mixed calls (i.e., biphonations with both sound elements produced simultaneously), although preliminary evidence has suggested that such vocalizations are individually distinctive and function as contact calls. Here we provide evidence that supports this notion in narwhal mother-calf communication. A female narwhal was tagged as part of larger studies on the life history and acoustic behavior of narwhals. At the time of tagging, it became apparent that the female had a calf, which remained close by during the tagging event. We found that the narwhal mother produced a distinct, highly stereotyped mixed call when separated from her calf and immediately after release from capture, which we interpret as preliminary evidence for contact call use between the mother and her calf. The mother’s mixed call production occurred continually over the 4.2 day recording period in addition to a second prominent but different stereotyped mixed call which we believe belonged to the narwhal calf. Thus, narwhal mothers produce highly stereotyped contact calls when separated from their calves, and it appears that narwhal calves similarly produce distinct, stereotyped mixed calls which we hypothesize also contribute to maintaining mother-calf contact. We compared this behavior to the acoustic behavior of two other adult females without calves, but also each with a unique, stereotyped call type. While we provide additional support for individual distinctiveness across narwhal contact calls, more research is necessary to determine whether these calls are vocal signatures which broadcast identity.

Lesser spot-nosed monkeys coordinate alarm call production with associated Campbell’s monkeys

Forest monkeys often form semi-permanent mixed-species associations to increase group-size related anti-predator benefits without corresponding increases in resource competition. In this study, we analysed the alarm call system of lesser spot-nosed monkeys, a primate that spends most of its time in mixed-species groups while occupying the lowest and presumably most dangerous part of the forest canopy. In contrast to other primate species, we found no evidence for predator-specific alarm calls. Instead, males gave one general alarm call type (‘kroo’) to three main dangers (i.e., crowned eagles, leopards and falling trees) and a second call type (‘tcha-kow’) as a coordinated response to calls produced in non-predatory contexts (‘boom’) by associated male Campbell’s monkeys. Production of ‘kroo’ calls was also strongly affected by the alarm calling behaviour of male Campbell’s monkeys, suggesting that male lesser spot-nosed monkeys adjust their alarm call production to another species’ vocal behaviour. We discuss different hypotheses for this unusual phenomenon and propose that high predation pressure can lead to reliance on other species vocal behaviour to minimise predation. Significance statement Predation can lead to the evolution of acoustically distinct, predator-specific alarm calls. However, there are occasional reports of species lacking such abilities, despite diverse predation pressure, suggesting that evolutionary mechanisms are more complex. We conducted field experiments to systematically describe the alarm calling behaviour of lesser spot-nosed monkeys, an arboreal primate living in the lower forest strata where pressure from different predators is high. We found evidence for two acoustically distinct calls but, contrary to other primates in the same habitat, no evidence for predator-specific alarms. Instead, callers produced one alarm call type (‘kroo’) to all predator classes and another call type (‘tcha-kow’) to non-predatory dangers, but only as a response to a specific vocalisation of Campbell’s monkeys (‘boom’). The production of both calls was affected by the calling behaviour of Campbell’s monkeys, suggesting that lesser spot-nosed monkey vocal behaviour is dependent on the antipredator behaviour of other species. Our study advances the theory of interspecies interactions and evolution of alarm calls.

The energetics of social signaling during roost location in Spix's disc-winged bats

Long-term social aggregations are maintained by multiple mechanisms, including the use of acoustic signals, which may nonetheless entail significant energetic costs. To date, however, no studies have gauged whether there are significant energetic costs to social call production in bats, which heavily rely on acoustic communication for a diversity of social tasks. We measure energetic expenditure during acoustic signaling in Spix's disc-winged bats (Thyroptera tricolor), a species that commonly uses contact calls to locate the ephemeral furled leaves that they use for roosting. To determine the cost of sound production, we measured oxygen consumption using intermittent-flow respirometry methods, with and without social signaling. Our results show that the emission of contact calls significantly increases oxygen consumption; vocal individuals spent, on average, 12.42 kJ more during social signaling trials than they spent during silent trials. We also found that as resting metabolic rates increased in males, there was a decreasing probability that they would emit response calls. These results provide support to the “allocation model”, which predicts that only individuals with lower self-maintenance costs can afford to spend energy in additional activities. Our results provide a step forward in our understanding of how physiology modulates behavior, specifically how the costs of call production and resting metabolic rates may explain the differences in vocal behavior among individuals.

Previously unknown behavior in parasitic cuckoo females: male-like vocalization during migratory activity

Background In the last decade, enigmatic male-like cuckoo calls have been reported several times in East Asia. These calls exhibited a combination of vocal traits of both Oriental Cuckoo (Cuculus optatus) and Common Cuckoo (Cuculus canorus) advertising calls, and some authors therefore suggested that the enigmatic calls were produced by either Common × Oriental Cuckoo male hybrids or Common Cuckoo males having a gene mutation. However, the exact identity of calling birds are still unknown. Methods We recorded previously unknown male-like calls from three captive Oriental Cuckoo females, and compared these calls with enigmatic vocalizations recorded in the wild as well as with advertising vocalizations of Common and Oriental Cuckoo males. To achieve this, we measured calls automatically. Besides, we video-recorded captive female emitting male-like calls, and compared these recordings with the YouTube recordings of calling males of both Common and Oriental Cuckoos to get insight into the mechanism of call production. Results The analysis showed that female male-like calls recorded in captivity were similar to enigmatic calls recorded in the wild. Therefore, Oriental Cuckoo females might produce the latter calls. Two features of these female calls appeared to be unusual among birds. First, females produced male-like calls at the time of spring and autumn migratory activity and on migration in the wild. Because of this, functional significance of this call remained puzzling. Secondly, the male-like female call unexpectedly combined features of both closed-mouth (closed beak and simultaneous inflation of the ‘throat sac’) and open-mouth (prominent harmonic spectrum and the maximum neck extension observed at the beginning of a sound) vocal behaviors. Conclusions The Cuculus vocalizations outside the reproductive season remain poorly understood. Here, we found for the first time that Oriental Cuckoo females can produce male-like calls in that time. Because of its rarity, this call might be an atavism. Indeed, female male-like vocalizations are still known in non-parasitic tropical and apparently more basal cuckoos only. Therefore, our findings may shed light on the evolution of vocal communication in avian brood parasites.

The energetics of social signaling during roost location in Spix’s disc-winged bats

Long-term social aggregations are maintained by multiple mechanisms, including the use of acoustic signals, which may nonetheless entail significant energetic costs. To date, however, no studies have gauged whether there are significant energetic costs to social call production in bats, which heavily rely on acoustic communication for a diversity of social tasks. We measure energetic expenditure during acoustic signaling in Spix’s disc-winged bats (Thyroptera tricolor), a species that commonly uses contact calls to locate the ephemeral furled leaves that they use for roosting. To determine the cost of sound production, we measured oxygen consumption using intermittent-flow respirometry methods, with and without social signaling. Our results show that the emission of contact calls significantly increases oxygen consumption; vocal individuals spent, on average, 12.42 kJ more during social signaling trials than they spent during silent trials. Furthermore, production of contact calls during longer periods increased oxygen consumption for males but not for females. We also found that as resting metabolic rates increased in males, there was a decreasing probability that they would emit response calls. These results provide support to the “allocation model”, which predicts that only individuals with lower self-maintenance costs can afford to spend energy in additional activities. Our results provide a step forward in our understanding of how physiology modulates behavior, specifically how the costs of call production and resting metabolic rates may explain the differences in vocal behavior among individuals.Summary StatementSpix’s disc-winged bats constantly produce contact calls while searching for roosts, which we show significantly increases an individual’s metabolic rate.