Vocal turn-taking in a non-human primate is learned during ontogeny

Conversational turn-taking is an integral part of language development, as it reflects a confluence of social factors that mitigate communication. Humans coordinate the timing of speech based on the behaviour of another speaker, a behaviour that is learned during infancy. While adults in several primate species engage in vocal turn-taking, the degree to which similar learning processes underlie its development in these non-human species or are unique to language is not clear. We recorded the natural vocal interactions of common marmosets (Callithrix jacchus) occurring with both their sibling twins and parents over the first year of life and observed at least two parallels with language development. First, marmoset turn-taking is a learned vocal behaviour. Second, marmoset parents potentially played a direct role in guiding the development of turn-taking by providing feedback to their offspring when errors occurred during vocal interactions similarly to what has been observed in humans. Though species-differences are also evident, these findings suggest that similar learning mechanisms may be implemented in the ontogeny of vocal turn-taking across our Order, a finding that has important implications for our understanding of language evolution.     

Individuality in a contact call of the ringtailed lemur (Lemur catta)

A vocalization of the ringtailed lemur (Lemur catta) was examined for individual differences according to several temporal- and frequency-dependent variables. Vocalizations were tape recorded at the Duke University Primate Center (Durham, NC) and spectrographically analyzed. Significant differences were found in pair-wise comparisons of call structure among the study subjects, thus providing the physical basis for individual discrimination. A separate analysis comparing degree of kinship and vocal similarity revealed a positive but nonsignificant correlation between these two variables. This study represents an initial examination of vocal individuality in prosimian primates.     

Insights from social transmission of information in rodents

Direct exposure to stimuli in their environment is not the only way that animals learn about important information. Individuals can infer fear from a social context through observation. Like humans, rats are very social animals, and may learn to infer information about their environment through their interactions with conspecifics. Here, we first review different models for social transmission of information in rodents. Second, we examine different modes of communication that are important to social learning. Then, we cover the different proximate factors that are thought to modulate the social transmission of information. Next, we identify social and environmental conditions that impact social learning, and finally, we conclude by revisiting social transmission through the lens of the Tinbergen framework.     

Social learning of a communicative signal in captive chimpanzees

The acquisition of linguistic competency from more experienced social partners is a fundamental aspect of human language. However, there is little evidence that non-human primates learn to use their vocalizations from social partners. Captive chimpanzees (Pan troglodytes) produce idiosyncratic vocal signals that are used intentionally to capture the attention of a human experimenter. Interestingly, not all apes produce these sounds, and it is unclear what factors explain this difference. We tested the hypothesis that these attention-getting (AG) sounds are socially learned via transmission between mothers and their offspring. We assessed 158 chimpanzees to determine if they produced AG sounds. A significant association was found between mother and offspring sound production. This association was attributable to individuals who were raised by their biological mother-as opposed to those raised by humans in a nursery environment. These data support the hypothesis that social learning plays a role in the acquisition and use of communicative vocal signals in chimpanzees.     

Contact call diversity in natural beluga entrapments in an Arctic estuary: Preliminary evidence of vocal signatures in wild belugas

Broadband, pulsed contact calls have been described for captive and temporarily restrained belugas, but little information exists on their usage in the wild. We examined vocal production during 14 natural beluga entrapments in a shallow channel in Cunningham Inlet, as isolation events offer ideal contexts to study contact calls. Drone footage, overhead photos, and shore‐based photos confirmed the number of individuals and age composition in each entrapment. Contact calls comprised the majority (61%) of vocalizations produced by entrapped whales compared to the free‐ranging herd (10%). We divided contact calls into complex (80%), those with a stereotyped, spectrographically prominent component overlapping the pulse train that characterizes all beluga contact calls, and simple (20%), those with no overlapping component. For each entrapment, we generated a catalogue of complex contact call types, totaling 87 types. Our classification was corroborated both quantitatively and by 55 naïve human judges. Occasional instances of overlapping contact calls of the same type indicated dyadic production. The number of contact call types per entrapment was strongly related to (never exceeding) the number of individuals, excluding neonates. Although this suggests a system of vocal signatures in belugas, consistent with their fission‐fusion society and earlier findings, whether signature identity is encoded individually or shared with related animals remains unknown.     

Horizontal transmission of the father's song in the zebra finch (Taeniopygia guttata)

As is the case for human speech, birdsong is transmitted across generations by imitative learning. Although transfer of song patterns from adults to juveniles typically occurs via vertical or oblique transmission, there is also evidence of horizontal transmission between juveniles of the same generation. Here, we show that a young male zebra finch (Taeniopygia guttata) that has been exposed to its father during the sensitive period for song learning can lead a brother, that has never heard the paternal song, to imitate some sounds of the father. Moreover, song similarity between the two brothers was higher than the similarity measured between the paternal song and the song of the brother that had a week-long exposure to the father. We speculate that the phenomenon of within-generation song learning among juveniles may be more widespread than previously thought and that when a juvenile evaluates potential models for imitative learning, a sibling may be as salient as an adult.     

Processes underlying complex patterns of song trait evolution in a Setophaga hybrid zone

During secondary contact between two species when hybrids are less fit than parents, mating signals are expected to diverge, while aggressive signals are expected to converge. If a single signal trait is used in both mating and aggression, then the dynamics between these two forces could influence the evolutionary trajectory of that trait. We studied such a situation in an avian hybrid zone between two Setophaga species, where birdsong is used in both mate attraction and territory defense. We hypothesized that song modules of the two species will show separate and distinct geographic patterns due to the influence of selective pressures for effective territorial aggression and for effective mate attraction. We conducted geographic cline analyses and playback experiments across this hybrid zone. We found an unexpected geographic pattern of asymmetric introgression of song rhythm, which may be explained by results of the playback experiments that suggest that differences in song rhythm serve a greater role in mate attraction than in territory defense. In contrast, differences in syllable morphology show little evidence of importance in mate attraction or territorial defense. Song features converge in the hybrid zone, yet patterns of trait change suggest that the song production modules may vary in their modes of development and inheritance. Syringeal motor gesturing, which gives rise to syllable morphology, shows a nonclinal mosaic pattern, suggesting that this trait may be predominantly learned. In contrast, respiratory patterning, which forms song rhythm, shows a clinal geographic transition, suggesting that this trait could be more innate. The results indicate that opposing forces act independently on song via distinct modules of the song production mechanism, driving complex patterns of song trait evolution.     

Role of a telencephalic nucleus in the delayed song learning of socially isolated zebra finches

Male zebra finches normally learn their song from adult models during a restricted period of juvenile development. If song models are not available then, juveniles develop an isolate song which can be modified in adulthood. In this report we investigate the features of juvenile experience that underly the timing of song learning. Juvenile males raised in soundproof chambers or in visual isolation from conspecifics developed stable isolate song. However, whereas visual isolate song notes were similar to those of colony-reared males, soundproof chamber isolates included many phonologically abnormal notes in their songs. Despite having stable isolate songs, both groups copied new notes from tutors presented to them in adulthood (2.7 notes per bird for soundproof chamber isolates, 4.4 notes per bird for visual isolates). Old notes were often modified or eliminated. We infer that social interactions with live tutors are normally important for closing the sensitive period for song learning. Lesions of a forebrain nucleus (IMAN) had previously been shown to disrupt juvenile song learning, but not maintenance of adult song for up to 5 weeks after surgery. In this study, colony-reared adult males given bilateral lesions of IMAN retained all their song notes for up to 4–7.5 months after lesioning. However, similar lesions blocked all song note acquisition in adulthood by both visual and soundproof chamber isolates. Other work has shown that intact hearing is necessary for the maintenance of adult zebra finch song. We infer that auditory pathways used for song maintenance and acquisition differ: IMAN is necessary for auditorily guided song acquisition—whether by juveniles or adults—but not for adult auditorily guided song maintenance. © 1993 John Wiley & Sons, Inc.     

Vertical Stratification and Caloric Content of the Standing Fruit Crop in a Tropical Lowland Forest1

Fruit abundance in tropical forests thus far has been studied in relation to consumer populations. Area–based surveys that focus on the quantity and quality of the standing fruit crop of an entire plant community, however, are lacking. This paper presents the results of a four–month study on the seasonality and vertical distribution of the standing fruit crop within a tropical forest during the dry season in southern Venezuela. Fruit numbers ranged from 262,000 to 424,000 fruits/ha. The standing crop was between 39 and 92 kg/ha, yielding 67,000 to 126,000 kj. Fruits were not evenly distributed in different forest layers. They were most abundant in the canopy above 16 m and scarce between 4 and 12 m above the ground. Despite a scarcity of fruits in the mid–strata, the caloric value of the total fruit supply peaked within a narrow layer of subcanopy at 12 to 16 m above ground due to a high amount of energy per fruit. Palms fruited mostly in this layer, their fruits contributing 59 percent of the energy supplied by all fruits. Above 12 m, we found a broader range of fruit sizes than in the forest below 12m. Small–sized fruits were distributed in the understory and in the canopy but were nearly absent from die mid–story. Corresponding to the abundance of small–sized fruits in the canopy, small frugivorous species, such as members of the Thraupidae, limited their foraging to the canopy strata whereas larger avian frugivores foraged mainly in die mid–story.     

Acquisition of a socially learned tool use sequence in chimpanzees: Implications for cumulative culture

Cumulative culture underpins humanity's enormous success as a species. Claims that other animals are incapable of cultural ratcheting are prevalent, but are founded on just a handful of empirical studies. Whether cumulative culture is unique to humans thus remains a controversial and understudied question that has far-reaching implications for our understanding of the evolution of this phenomenon. We investigated whether one of human's two closest living primate relatives, chimpanzees, are capable of a degree of cultural ratcheting by exposing captive populations to a novel juice extraction task. We found that groups (N = 3) seeded with a model trained to perform a tool modification that built upon simpler, unmodified tool use developed the seeded tool method that allowed greater juice returns than achieved by groups not exposed to a trained model (non-seeded controls; N = 3). One non-seeded group also discovered the behavioral sequence, either by coupling asocial and social learning or by repeated invention. This behavioral sequence was found to be beyond what an additional control sample of chimpanzees (N = 1 group) could discover for themselves without a competent model and lacking experience with simpler, unmodified tool behaviors. Five chimpanzees tested individually with no social information, but with experience of simple unmodified tool use, invented part, but not all, of the behavioral sequence. Our findings indicate that (i) social learning facilitated the propagation of the model-demonstrated tool modification technique, (ii) experience with simple tool behaviors may facilitate individual discovery of more complex tool manipulations, and (iii) a subset of individuals were capable of learning relatively complex behaviors either by learning asocially and socially or by repeated invention over time. That chimpanzees learn increasingly complex behaviors through social and asocial learning suggests that humans' extraordinary ability to do so was built on such prior foundations.     

Vocal convergence in a multi-level primate society: insights into the evolution of vocal learning

The extent to which nonhuman primate vocalizations are amenable to modification through experience is relevant for understanding the substrate from which human speech evolved. We examined the vocal behaviour of Guinea baboons, Papio papio, ranging in the Niokolo Koba National Park in Senegal. Guinea baboons live in a multi-level society, with units nested within parties nested within gangs. We investigated whether the acoustic structure of grunts of 27 male baboons of two gangs varied with party/gang membership and genetic relatedness. Males in this species are philopatric, resulting in increased male relatedness within gangs and parties. Grunts of males that were members of the same social levels were more similar than those of males in different social levels (N = 351 dyads for comparison within and between gangs, and N = 169 dyads within and between parties), but the effect sizes were small. Yet, acoustic similarity did not correlate with genetic relatedness, suggesting that higher amounts of social interactions rather than genetic relatedness promote the observed vocal convergence. We consider this convergence a result of sensory–motor integration and suggest this to be an implicit form of vocal learning shared with humans, in contrast to the goal-directed and intentional explicit form of vocal learning unique to human speech acquisition.     

Vocal matching and intensity of begging calls are associated with a forebrain song circuit in a generalist brood parasite

Vocalizations produced by developing young early in life have simple acoustic features and are thought to be innate. Complex forms of early vocal learning are less likely to evolve in young altricial songbirds because the forebrain vocal‐learning circuit is underdeveloped during the period when early vocalizations are produced. However, selective pressure experienced in early postnatal life may lead to early vocal learning that is likely controlled by a simpler brain circuit. We found the food begging calls produced by fledglings of the brown‐headed cowbird (Molothrus ater), a generalist avian brood parasite, induced the expression of several immediate early genes and early circuit innervation in a forebrain vocal‐motor pathway that is later used for vocal imitation. The forebrain neural activity was correlated with vocal intensity and variability of begging calls that appears to allow cowbirds to vocally match host nestmates. The begging‐induced forebrain circuits we observed in fledgling cowbirds were not detected in nonparasitic passerines, including species that are close relatives to the cowbird. The involvement of forebrain vocal circuits during fledgling begging and its association with vocal learning plasticity may be an adaptation that provides young generalist brood parasites with a flexible signaling strategy to procure food from a wide range of heterospecific host parents. © 2015 Wiley Periodicals, Inc. Develop Neurobiol 76: 615–625, 2016     

Vertical vs. horizontal transmission of the microbiome in a key disease vector,Ixodes pacificus

Vector‐borne pathogens are increasingly found to interact with the vector's microbiome, influencing disease transmission dynamics. However, the processes that regulate the formation and development of the microbiome are largely unexplored for most tick species, an emerging group of disease vectors. It is not known how much of the tick microbiome is acquired through vertical transmission vs. horizontally from the environment or interactions with bloodmeal sources. Using 16S rRNA sequencing, we examined the microbiome of Ixodes pacificus, the vector of Lyme disease in the western USA, across life stages and infection status. We also characterized microbiome diversity in field and laboratory‐collected nymphal ticks to determine how the surrounding environment affects microbiome diversity. We found a decrease in both species richness and evenness as the tick matures from larva to adult. When the dominant Rickettsial endosymbiont was computationally removed from the tick microbial community, we found that infected nymphs had lower species evenness than uninfected ticks, suggesting that lower microbiome diversity is associated with pathogen transmission in wild‐type ticks. Furthermore, laboratory‐reared nymph microbiome diversity was found to be compositionally distinct and significantly depauperate relative to field‐collected nymphs. These results highlight unique patterns in the microbial community of I. pacificus that is distinct from other tick species. We provide strong evidence that ticks acquire a significant portion of their microbiome through exposure to their environment despite a loss of overall diversity through life stages. We provide evidence that loss of microbial diversity is at least in part due to elimination of microbial diversity with bloodmeal feeding but other factors may also play a role.     

Habitat filtering influences the phylogenetic structure of avian communities across a coastal gradient in southern Brazil

The evolution of a particular trait or combination of traits within lineages may affect subsequent evolutionary outcomes, leading closely related species to exhibit higher phenotypic similarity than expected under a simple Brownian‐motion evolutionary model. Niche theory postulates that phenotypes determine species distribution across environmental gradients, leading to a phylogenetic signature in the community assembly. Thus, the incorporation of species phylogeny in the analysis of community ecology structure allows one to link broader environmental, spatial and temporal factors to local, small‐scale ecological processes, thus enabling understanding of community assembly patterns in a broader context. We used the net relatedness index to assess phylogenetic structure within avian communities across a harshness gradient in coastal habitats in southern Brazil. We also evaluated phylogenetic beta diversity, to test whether closely related species exploit habitats with similar environmental conditions. In order to do so, we scaled up phylogenetic information from the species to site level using phylogenetic fuzzy weighting. We found a pattern of phylogenetic clustering in less‐vegetated habitats, namely sandy beach and dunes, which are subject to harsher conditions because of proximity to the ocean. Basal lineages were associated with the more structurally homogeneous sandy beach, while late‐divergence clades occurred in more complex habitats, which were positively related to vegetation cover and height. The observed pattern of phylogenetic clustering suggested the importance of harsh conditions in constraining the distribution of avian lineages. Furthermore, contrasting environmental features between habitats influenced phylogenetic variation, demonstrating the prevalence of phylogenetic habitat filtering. From an applied point of view, such as planning and management of biological reserves, we showed that the full array of habitat patches embedded within coastal ecological gradients must be included in order to preserve distinct evolutionary lineages.     

Rapid synaptic plasticity contributes to a learned conjunctive code of position and choice-related information in the hippocampus

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No evidence for memory retention of a learned association between a cue and roost quality after hibernation in free-ranging bats

Hibernation is a physiological adaptation that allows animals to survive adverse environmental conditions. A commonly assumed cost of hibernation is impaired memory retention. So far, however, the effects of hibernation on memory retention have been assessed on only a few behavioral tasks, and exclusively under laboratory conditions. Taking advantage of the longevity and strict colony fidelity of female Bechstein's bats, we were able to evaluate memory retention in the same individuals over two consecutive summers in the field. We used a pairwise roost choice experiment with automatic monitoring of RFID-tagged bats. Roosts’ suitability as day roost was associated with a distinctive external echo-acoustic cue. Experiments were separated by a natural hibernation period of eight months. We determined associative learning and memory retention by comparing the bats’ proportion of visits to suitable roosts within and between breeding seasons, respectively. During the first breeding season, bats quickly learned to associate the suitable roosts with their external cue. After hibernating, we found no evidence that individuals remembered the association between the roosts’ suitability and their respective external cue, suggesting a lack of memory retention. Nevertheless, bats quickly re-learned the same association during the second breeding season, emphasizing the high behavioral flexibility of Bechstein's bats.