Call combination in African forest elephants Loxodonta cyclotis.

Syntax, the combination of meaning-devoid phonemes into meaningful words, which in turn are combined in structurally and semantically complex sentences, is fundamental to the unlimited expressiveness of human languages. Studying the functions of call combinations in non-human species provides insights into the evolution of such syntactic capabilities. Here, we investigated the combination of high amplitude broadband calls with low frequency rumble vocalizations in a highly social species, the African forest elephant Loxodonta cyclotis. Rumbles play an integral role in coordinating social interactions by transmitting socially relevant information, including individual identity. By contrast, broadband calls, such as roars, are thought to function as signals of distress and urgency as they are typically produced in situations of high emotional intensity. Functional changes associated with the combination of these calls remain little understood. We found that call combinations were produced by all age-sex classes but were most prevalent in immature individuals. We found that rumbles used singularly occurred in all five investigated social contexts, whereas single broadband calls were restricted to two resource-related contexts. Call combinations also occurred in all five contexts, suggesting an increase in the functional use of broadband calls when combined with rumbles, analogous to the generativity brought about through syntax in human speech. Moreover, combining calls appeared to lead to functional shifts towards high-stake contexts. Call combinations were more likely in competition contexts compared to single rumbles, and more likely in separation contexts compared to single broadband calls. We suggest that call combination in forest elephants may aide to reduce message ambiguity in high-stake situation by simultaneously communicating distress and individual identity, which may be critical to secure access to resources, reduce the risk of injury and to reunite with or recruit the support of the family group.

Population dynamics and genetic connectivity in recent chimpanzee history.

Knowledge on the population history of endangered species is critical for conservation, but whole-genome data on chimpanzees (Pan troglodytes) is geographically sparse. Here, we produced the first non-invasive geolocalized catalog of genomic diversity by capturing chromosome 21 from 828 non-invasive samples collected at 48 sampling sites across Africa. The four recognized subspecies show clear genetic differentiation correlating with known barriers, while previously undescribed genetic exchange suggests that these have been permeable on a local scale. We obtained a detailed reconstruction of population stratification and fine-scale patterns of isolation, migration, and connectivity, including a comprehensive picture of admixture with bonobos (Pan paniscus). Unlike humans, chimpanzees did not experience extended episodes of long-distance migrations, which might have limited cultural transmission. Finally, based on local rare variation, we implement a fine-grained geolocalization approach demonstrating improved precision in determining the origin of confiscated chimpanzees.

Does Social Complexity Drive Vocal Complexity? Insights from the Two African Elephant Species.

The social complexity hypothesis (SCH) for communication states that the range and frequency of social interactions drive the evolution of complex communication systems. Surprisingly, few studies have empirically tested the SHC for vocal communication systems. Filling this gap is important because a co-evolutionary runaway process between social and vocal complexity may have shaped the most intricate communication system, human language. We here propose the African elephant Loxodonta spec. as an excellent study system to investigate the relationships between social and vocal complexity. We review how the distinct differences in social complexity between the two species of African elephants, the forest elephant L. cyclotis and the savanna elephant L. africana, relate to repertoire size and structure, as well as complex communication skills in the two species, such as call combination or intentional formant modulation including the trunk. Our findings suggest that Loxodonta may contradict the SCH, as well as other factors put forth to explain patterns of vocal complexity across species. We propose that life history traits, a factor that has gained little attention as a driver of vocal complexity, and the extensive parental care associated with a uniquely low and slow reproductive rate, may have led to the emergence of pronounced vocal complexity in the forest elephant despite their less complex social system compared to the savanna elephant. Conclusions must be drawn cautiously, however. A better understanding of vocal complexity in the genus Loxodonta will depend on continuing advancements in remote data collection technologies to overcome the challenges of observing forest elephants in their dense rainforest habitat, as well as the availability of directly comparable data and methods, quantifying both structural and contextual variability in the production of rumbles and other vocalizations in both species of African elephants.

Dominance style is a key predictor of vocal use and evolution across nonhuman primates.

Animal communication has long been thought to be subject to pressures and constraints associated with social relationships. However, our understanding of how the nature and quality of social relationships relates to the use and evolution of communication is limited by a lack of directly comparable methods across multiple levels of analysis. Here, we analysed observational data from 111 wild groups belonging to 26 non-human primate species, to test how vocal communication relates to dominance style (the strictness with which a dominance hierarchy is enforced, ranging from 'despotic' to 'tolerant'). At the individual-level, we found that dominant individuals who were more tolerant vocalized at a higher rate than their despotic counterparts. This indicates that tolerance within a relationship may place pressure on the dominant partner to communicate more during social interactions. At the species-level, however, despotic species exhibited a larger repertoire of hierarchy-related vocalizations than their tolerant counterparts. Findings suggest primate signals are used and evolve in tandem with the nature of interactions that characterize individuals' social relationships.

Quantitative estimates of glacial refugia for chimpanzees (Pan troglodytes) since the Last Interglacial (120,000 BP).

Paleoclimate reconstructions have enhanced our understanding of how past climates have shaped present-day biodiversity. We hypothesize that the geographic extent of Pleistocene forest refugia and suitable habitat fluctuated significantly in time during the late Quaternary for chimpanzees (Pan troglodytes). Using bioclimatic variables representing monthly temperature and precipitation estimates, past human population density data, and an extensive database of georeferenced presence points, we built a model of changing habitat suitability for chimpanzees at fine spatio-temporal scales dating back to the Last Interglacial (120,000 BP). Our models cover a spatial resolution of 0.0467° (approximately 5.19 km2 grid cells) and a temporal resolution of between 1000 and 4000 years. Using our model, we mapped habitat stability over time using three approaches, comparing our modeled stability estimates to existing knowledge of Afrotropical refugia, as well as contemporary patterns of major keystone tropical food resources used by chimpanzees, figs (Moraceae), and palms (Arecacae). Results show habitat stability congruent with known glacial refugia across Africa, suggesting their extents may have been underestimated for chimpanzees, with potentially up to approximately 60,000 km2 of previously unrecognized glacial refugia. The refugia we highlight coincide with higher species richness for figs and palms. Our results provide spatio-temporally explicit insights into the role of refugia across the chimpanzee range, forming the empirical foundation for developing and testing hypotheses about behavioral, ecological, and genetic diversity with additional data. This methodology can be applied to other species and geographic areas when sufficient data are available.

Recent genetic connectivity and clinal variation in chimpanzees.

Much like humans, chimpanzees occupy diverse habitats and exhibit extensive behavioural variability. However, chimpanzees are recognized as a discontinuous species, with four subspecies separated by historical geographic barriers. Nevertheless, their range-wide degree of genetic connectivity remains poorly resolved, mainly due to sampling limitations. By analyzing a geographically comprehensive sample set amplified at microsatellite markers that inform recent population history, we found that isolation by distance explains most of the range-wide genetic structure of chimpanzees. Furthermore, we did not identify spatial discontinuities corresponding with the recognized subspecies, suggesting that some of the subspecies-delineating geographic barriers were recently permeable to gene flow. Substantial range-wide genetic connectivity is consistent with the hypothesis that behavioural flexibility is a salient driver of chimpanzee responses to changing environmental conditions. Finally, our observation of strong local differentiation associated with recent anthropogenic pressures portends future loss of critical genetic diversity if habitat fragmentation and population isolation continue unabated.

Comparative bioacoustics: a roadmap for quantifying and comparing animal sounds across diverse taxa.

Animals produce a wide array of sounds with highly variable acoustic structures. It is possible to understand the causes and consequences of this variation across taxa with phylogenetic comparative analyses. Acoustic and evolutionary analyses are rapidly increasing in sophistication such that choosing appropriate acoustic and evolutionary approaches is increasingly difficult. However, the correct choice of analysis can have profound effects on output and evolutionary inferences. Here, we identify and address some of the challenges for this growing field by providing a roadmap for quantifying and comparing sound in a phylogenetic context for researchers with a broad range of scientific backgrounds. Sound, as a continuous, multidimensional trait can be particularly challenging to measure because it can be hard to identify variables that can be compared across taxa and it is also no small feat to process and analyse the resulting high-dimensional acoustic data using approaches that are appropriate for subsequent evolutionary analysis. Additionally, terminological inconsistencies and the role of learning in the development of acoustic traits need to be considered. Phylogenetic comparative analyses also have their own sets of caveats to consider. We provide a set of recommendations for delimiting acoustic signals into discrete, comparable acoustic units. We also present a three-stage workflow for extracting relevant acoustic data, including options for multivariate analyses and dimensionality reduction that is compatible with phylogenetic comparative analysis. We then summarize available phylogenetic comparative approaches and how they have been used in comparative bioacoustics, and address the limitations of comparative analyses with behavioural data. Lastly, we recommend how to apply these methods to acoustic data across a range of study systems. In this way, we provide an integrated framework to aid in quantitative analysis of cross-taxa variation in animal sounds for comparative phylogenetic analysis. In addition, we advocate the standardization of acoustic terminology across disciplines and taxa, adoption of automated methods for acoustic feature extraction, and establishment of strong data archival practices for acoustic recordings and data analyses. Combining such practices with our proposed workflow will greatly advance the reproducibility, biological interpretation, and longevity of comparative bioacoustic studies.

An exploration of Menzerath's law in wild mountain gorilla vocal sequences.

Menzerath's law, traditionally framed as a negative relationship between the size of a structure and its constituent parts (e.g. sentences with more clauses have shorter clauses), is widespread across information-coding systems ranging from human language and the vocal and gestural sequences of primates and birds, to the building blocks of DNA, genes and proteins. Here, we analysed an extensive dataset of 'close-call' sequences produced by wild mountain gorillas (Gorilla beringei beringei, no. individuals = 10, no. sequences = 2189) to determine whether, in accordance with Menzerath's law, a negative relationship existed between the number of vocal units in a sequence and the duration of its constituent units. We initially found positive evidence for this but, on closer inspection, the negative relationship was driven entirely by the difference between single- and multi-unit (two to six unit) sequences. Once single-unit sequences were excluded from the analysis, we identified a relationship in the opposite direction, with longer sequences generally composed of longer units. The close-call sequences of mountain gorillas therefore represent an intriguing example of a non-human vocal system that only partially conforms to the predictions of Menzerath's law.

Environmental variability supports chimpanzee behavioural diversity.

Large brains and behavioural innovation are positively correlated, species-specific traits, associated with the behavioural flexibility animals need for adapting to seasonal and unpredictable habitats. Similar ecological challenges would have been important drivers throughout human evolution. However, studies examining the influence of environmental variability on within-species behavioural diversity are lacking despite the critical assumption that population diversification precedes genetic divergence and speciation. Here, using a dataset of 144 wild chimpanzee (Pan troglodytes) communities, we show that chimpanzees exhibit greater behavioural diversity in environments with more variability - in both recent and historical timescales. Notably, distance from Pleistocene forest refugia is associated with the presence of a larger number of behavioural traits, including both tool and non-tool use behaviours. Since more than half of the behaviours investigated are also likely to be cultural, we suggest that environmental variability was a critical evolutionary force promoting the behavioural, as well as cultural diversification of great apes.

Classification of Florida manatee (Trichechus manatus latirostris) vocalizations.

The vocal repertoire for the Florida manatee is quantitatively categorized from a sample of 1114 calls recorded from 3 different manatee habitats in Florida. First, manatee vocalizations were categorized into five call categories based on visual inspection of spectrograms and following descriptions provided in previous studies. Second, based on measurements of 17 acoustic parameters, the subjective classification scheme was validated using classification and regression trees (CARTs) and model-based cluster analysis paired with silhouette coefficients. CART analysis revealed that these five broad call categories can be successfully distinguished based on correct classification scores of 41.6%-62.5%. Silhouette coefficients determined that the manatee vocal repertoire is highly intergraded. This study supports and expands upon existing subjective categorization schemes by providing a quantifiable methodology for describing the Florida manatees' vocal repertoire. These findings contribute to the increasing number of studies suggesting many animal species vocal repertoires contain graded call types.

Extracting physiological information in experimental biology via Eulerian video magnification.

BACKGROUND: Videographic material of animals can contain inapparent signals, such as color changes or motion that hold information about physiological functions, such as heart and respiration rate, pulse wave velocity, and vocalization. Eulerian video magnification allows the enhancement of such signals to enable their detection. The purpose of this study is to demonstrate how signals relevant to experimental physiology can be extracted from non-contact videographic material of animals. RESULTS: We applied Eulerian video magnification to detect physiological signals in a range of experimental models and in captive and free ranging wildlife. Neotenic Mexican axolotls were studied to demonstrate the extraction of heart rate signal of non-embryonic animals from dedicated videographic material. Heart rate could be acquired both in single and multiple animal setups of leucistic and normally colored animals under different physiological conditions (resting, exercised, or anesthetized) using a wide range of video qualities. Pulse wave velocity could also be measured in the low blood pressure system of the axolotl as well as in the high-pressure system of the human being. Heart rate extraction was also possible from videos of conscious, unconstrained zebrafish and from non-dedicated videographic material of sand lizard and giraffe. This technique also allowed for heart rate detection in embryonic chickens in ovo through the eggshell and in embryonic mice in utero and could be used as a gating signal to acquire two-phase volumetric micro-CT data of the beating embryonic chicken heart. Additionally, Eulerian video magnification was used to demonstrate how vocalization-induced vibrations can be detected in infrasound-producing Asian elephants. CONCLUSIONS: Eulerian video magnification provides a technique to extract inapparent temporal signals from videographic material of animals. This can be applied in experimental and comparative physiology where contact-based recordings (e.g., heart rate) cannot be acquired.

Acoustic structure of forest elephant rumbles: a test of the ambiguity reduction hypothesis.

Quantitative assessments of the structure of vocalizations are a fundamental prerequisite to understand a species' vocal communication system and, more broadly, the selective pressures shaping vocal repertoires. For example, to reduce ambiguity in signal interpretation in the absence of auxiliary visual cues, species in densely vegetated habitats should exhibit more discrete vocal signals than species in open habitats. To test this "ambiguity reduction hypothesis", we conducted the first quantitative assessment of the rumble vocalizations of the forest elephant. Based on 686 forest elephant rumbles recorded with autonomous acoustic recording units at four sites across Central Africa, we used model-based cluster analyses paired with subsequent evaluation of cluster-discreteness and discriminant function analyses to quantify the structure of rumbles based on 23 source- and filter-related acoustic parameters. Model-based cluster analyses suggest that rumbles can be classified into five to eight types. Similar to previous findings in savannah elephants and contrary to the ambiguity reduction hypothesis, average silhouette coefficients below 0.34 indicated that these rumble types were highly intergraded. However, discriminant function analyses predicted rumble types with at least 75% accuracy whereby the location of the minimum fundamental frequency, middle slope and peak frequency contributed most to separation between types. In line with an increasing number of studies highlighting that a distinction between discrete and graded repertoires may have little biological significance, we propose that ambiguity reduction may take place through the evolution of perceptual and cognitive mechanisms, rather than acting on vocal production.

Human impact erodes chimpanzee behavioral diversity.

Chimpanzees possess a large number of behavioral and cultural traits among nonhuman species. The "disturbance hypothesis" predicts that human impact depletes resources and disrupts social learning processes necessary for behavioral and cultural transmission. We used a dataset of 144 chimpanzee communities, with information on 31 behaviors, to show that chimpanzees inhabiting areas with high human impact have a mean probability of occurrence reduced by 88%, across all behaviors, compared to low-impact areas. This behavioral diversity loss was evident irrespective of the grouping or categorization of behaviors. Therefore, human impact may not only be associated with the loss of populations and genetic diversity, but also affects how animals behave. Our results support the view that "culturally significant units" should be integrated into wildlife conservation.

Behavioral Variation in Gorillas: Evidence of Potential Cultural Traits.

The question of whether any species except humans exhibits culture has generated much debate, partially due to the difficulty of providing conclusive evidence from observational studies in the wild. A starting point for demonstrating the existence of culture that has been used for many species including chimpanzees and orangutans is to show that there is geographic variation in the occurrence of particular behavioral traits inferred to be a result of social learning and not ecological or genetic influences. Gorillas live in a wide variety of habitats across Africa and they exhibit flexibility in diet, behavior, and social structure. Here we apply the 'method of exclusion' to look for the presence/absence of behaviors that could be considered potential cultural traits in well-habituated groups from five study sites of the two species of gorillas. Of the 41 behaviors considered, 23 met the criteria of potential cultural traits, of which one was foraging related, nine were environment related, seven involved social interactions, five were gestures, and one was communication related. There was a strong positive correlation between behavioral dissimilarity and geographic distance among gorilla study sites. Roughly half of all variation in potential cultural traits was intraspecific differences (i.e. variability among sites within a species) and the other 50% of potential cultural traits were differences between western and eastern gorillas. Further research is needed to investigate if the occurrence of these traits is influenced by social learning. These findings emphasize the importance of investigating cultural traits in African apes and other species to shed light on the origin of human culture.

Chimpanzee accumulative stone throwing.

The study of the archaeological remains of fossil hominins must rely on reconstructions to elucidate the behaviour that may have resulted in particular stone tools and their accumulation. Comparatively, stone tool use among living primates has illuminated behaviours that are also amenable to archaeological examination, permitting direct observations of the behaviour leading to artefacts and their assemblages to be incorporated. Here, we describe newly discovered stone tool-use behaviour and stone accumulation sites in wild chimpanzees reminiscent of human cairns. In addition to data from 17 mid- to long-term chimpanzee research sites, we sampled a further 34 Pan troglodytes communities. We found four populations in West Africa where chimpanzees habitually bang and throw rocks against trees, or toss them into tree cavities, resulting in conspicuous stone accumulations at these sites. This represents the first record of repeated observations of individual chimpanzees exhibiting stone tool use for a purpose other than extractive foraging at what appear to be targeted trees. The ritualized behavioural display and collection of artefacts at particular locations observed in chimpanzee accumulative stone throwing may have implications for the inferences that can be drawn from archaeological stone assemblages and the origins of ritual sites.

Audience effects, but not environmental influences, explain variation in gorilla close distance vocalizations-A test of the acoustic adaptation hypothesis.

Close distance vocalizations are an integral part of primate vocal communication. They exhibit large acoustic variation which has been suggested to constitute flexible responses to the highly variable social setting of group living animals. However, a recent study suggested that acoustic variation in close distance calls of baboons may also arise from acoustic adaptations to environmental factors in order to counteract sound degradation. We tested whether the variation in calling rate and acoustic structure of gorilla close distance vocalizations may serve to counteract distorting effects of vegetation during sound propagation. Using focal animal sampling we recorded the vocal behavior of 15 adult individuals living in two groups: one group of western lowland gorillas Gorilla gorilla gorilla and one group of mountain gorillas Gorilla beringei beringei. We considered the distance between the caller and its nearest neighbor as the minimum transmission distance of calls; while vegetation density was quantified through measures of visibility. Our analysis revealed vocal plasticity in gorilla close calls in relation to changes in visibility and nearest neighbor distance. However, the observed changes in fundamental frequency and calling rate are unlikely to counteract degrading effects of vegetation, but rather seem to reflect reactions to variation in spatial and visual separation from other group members, similar to the audience effects demonstrated in a range of other species. We propose that vocal plasticity to counteract distorting environmental effects may not be prevalent across taxa and perhaps confined to species living in heterogeneous habitats with highly variable transmission conditions.

Contextual correlates of syntactic variation in mountain and western gorilla close-distance vocalizations: indications for lexical or phonological syntax?

The core of the generative power of human languages lies in our ability to combine acoustic units under specific rules into structurally complex and semantically rich utterances. While various animal species concatenate acoustic units into structurally elaborate vocal sequences, such compound calls do not appear to be compositional as their information content cannot be derived from the information content of each of its components. As such, animal compound calls are said to constitute a form of phonological syntax, as in the construction of words in human language, whereas evidence for rudimentary forms of lexical syntax, analogous to the construction of sentences out of words, is scarce. In a previous study, we demonstrated that the repertoire of close-distance calls of mountain and western gorillas consists of acoustic units that are either used singularly or non-randomly combined. Here, we investigate whether this syntactic variation provides indications for lexical or phonological syntax. Specifically, we examined the differences between the potential information content of compound calls and their components used singularly through investigating the contexts in which they are used. We found that the gorillas emitted compound calls in contexts similar to some but not all components, but also in a context rarely found for any of their components. As such, the investigated compound calls did not appear to be compositional as their information content cannot be derived from the information content of each of their components. Our results suggest that combining acoustic units into compound vocalizations by gorillas constitutes a form of phonological syntax, which may enable them to increase the number of messages that can be transmitted by an otherwise small repertoire of acoustic units.

Genetic architecture of tameness in a rat model of animal domestication.

A common feature of domestic animals is tameness-i.e., they tolerate and are unafraid of human presence and handling. To gain insight into the genetic basis of tameness and aggression, we studied an intercross between two lines of rats (Rattus norvegicus) selected over >60 generations for increased tameness and increased aggression against humans, respectively. We measured 45 traits, including tameness and aggression, anxiety-related traits, organ weights, and levels of serum components in >700 rats from an intercross population. Using 201 genetic markers, we identified two significant quantitative trait loci (QTL) for tameness. These loci overlap with QTL for adrenal gland weight and for anxiety-related traits and are part of a five-locus epistatic network influencing tameness. An additional QTL influences the occurrence of white coat spots, but shows no significant effect on tameness. The loci described here are important starting points for finding the genes that cause tameness in these rats and potentially in domestic animals in general.