A multifaceted framework to establish the presence of meaning in non-human communication.

Does non-human communication, like language, involve meaning? This question guides our focus through an interdisciplinary review of the theories and terminology used to study meaning across disciplines and species. Until now, it has been difficult to apply the concept of meaning to communication in non-humans. This is partly because of the varied approaches to the study of meaning. Additionally, while there is a scholarly acknowledgement of potential meaning in non-human cognition, there is also scepticism when the topic of communication arises. We organise some of the key literature into a coherent framework that can bridge disciplines and species, to ensure that aspects of meaning are accurately and fairly compared. We clarify the growing view in the literature that, rather than requiring multiple definitions or being split into different types, meaning is a multifaceted yet still unified concept. In so doing, we propose that meaning is an umbrella term. Meaning cannot be summed up with a short definition or list of features, but involves multiple complexities that are outlined in our framework. Specifically, three global facets are needed to describe meaning: a Signal Meaning Facet, an Interactant Meaning Facet, and a Resultant Meaning Facet. Most importantly, we show that such analyses are possible to apply as much to non-humans as to humans. We also emphasise that meaning nuances differ among non-human species, making a dichotomous approach to meaning questionable. Instead, we show that a multifaceted approach to meaning establishes how meaning appears within highly diverse examples of non-human communication, in ways consistent with the phenomenon's presence in human non-verbal communication and language(s). Therefore, without further recourse to 'functional' approaches that circumvent the critical question of whether any non-human meaning exists, we show that the concept of meaning is suitable for evolutionary biologists, behavioural ecologists, and others to study, to establish exactly which species exhibit meaning in their communication and in what ways.

Genetic distance from wolves affects family dogs' reactions towards howls.

Domestication dramatically changes behaviour, including communication, as seen in the case of dogs (Canis familiaris) and wolves (Canis lupus). We tested the hypothesis that domestication may affect an ancient, shared communication form of canids, the howling which seems to have higher individual variation in dogs: the perception and usage of howls may be affected by the genetic relatedness of the breeds to their last common ancestor with wolves ('root distance') and by other individual features like age, sex, and reproductive status. We exposed 68 purebred dogs to wolf howl playbacks and recorded their responses. We identified an interaction between root distance and age on the dogs' vocal and behavioural responses: older dogs from more ancient breeds responded longer with howls and showed more stress behaviours. Our results suggest that domestication impacts vocal behaviour significantly: disintegrating howling, a central, species-specific communication form of canids and gradually eradicating it from dogs' repertoire.

Sister species diverge in modality-specific courtship signal form and function.

Understanding the relative importance of different sources of selection (e.g., the environment, social/sexual selection) on the divergence or convergence of reproductive communication can shed light on the origin, maintenance, or even disappearance of species boundaries. Using a multistep approach, we tested the hypothesis that two presumed sister species of wolf spider with overlapping ranges and microhabitat use, yet differing degrees of sexual dimorphism, have diverged in their reliance on modality-specific courtship signaling. We predicted that male Schizocosa crassipalpata (no ornamentation) rely predominantly on diet-dependent vibratory signaling for mating success. In contrast, we predicted that male S. bilineata (black foreleg brushes) rely on diet-dependent visual signaling. We first tested and corroborated the sister-species relationship between S. crassipalpata and S. bilineata using phylogenomic scale data. Next, we tested for species-specific, diet-dependent vibratory and visual signaling by manipulating subadult diet and subsequently quantifying adult morphology and mature male courtship signals. As predicted, vibratory signal form was diet-dependent in S. crassipalpata, while visual ornamentation (brush area) was diet-dependent in S. bilineata. We then compared the species-specific reliance on vibratory and visual signaling by recording mating across artificially manipulated signaling environments (presence/absence of each modality in a 2 × 2 full factorial design). In accordance with our diet dependence results for S. crassipalpata, the presence of vibratory signaling was important for mating success. In contrast, the light and vibratory environment interacted to influence mating success in S. bilineata, with vibratory signaling being important only in the absence of light. We found no differences in overall activity patterns. Given that these species overlap in much of their range and microhabitat use, we suggest that competition for signaling space may have led to the divergence and differential use of sensory modalities between these sister species.

Tracking cryptic animals using acoustic multilateration: A system for long-range wolf detection.

The study of animal behavior in the wild requires the ability to locate and observe animals with the minimum disturbance to their natural behavior. This can be challenging for animals that avoid humans, are difficult to detect, or range widely between sightings. Global Positioning System (GPS) collars provide one solution but limited battery life, and the disturbance to the animal caused by capture and collaring can make this impractical in many applications. Wild wolves Canis lupus are an example of a species that is difficult to study in the wild, yet are of considerable conservation and management importance. This manuscript presents a system for accurately locating wolves using differences in the time of arrival of howl vocalizations at multiple recorders (multilateration), synchronized via GPS. This system has been deployed in Yellowstone National Park for two years and has recorded over 1200 instances of howling behavior. As most instances of howling occur at night, or when human observers are not physically present, the system provides location information that would otherwise be unavailable to researchers. The location of a vocalizing animal can, under some circumstances, be determined to within an error of approximately 20 m and at ranges up to 7 km.

The progression pattern of male hyrax songs and the role of climactic ending.

The study of animal vocal signals can either focus on the properties of distinct vocal elements or address the signal as a whole. Although some attention has been given to the continuous progression patterns of bird songs, such patterns in mammalian vocalisations have been largely overlooked. We examined temporal changes in structural and acoustic parameters in male rock hyrax songs. We found a gradual increase in call frequency and amplitude towards the song ending, as well as an abrupt increase in bout syntactic complexity, peaking in the last quintile of a song. In musical terms, such a pattern can be described as a crescendo (amplitude increase) with a terminal climax. In Western music, crescendos are used to maintain attention and direct the listeners towards a memorable highpoint of the musical piece. This structure may have an analogous function in animal communication, recruiting audience attention towards the climactic and potentially most informative part of the signal. Our playback experiments revealed that hyrax males tend to reply more to songs with a climactic ending, indicating that this progression pattern is important for hyrax communication. We suggest that animal vocal communication research can benefit from adding musical concepts to the analysis toolbox.

Visual classification of feral cat Felis silvestris catus vocalizations.

Cat vocal behavior, in particular, the vocal and social behavior of feral cats, is poorly understood, as are the differences between feral and fully domestic cats. The relationship between feral cat social and vocal behavior is important because of the markedly different ecology of feral and domestic cats, and enhanced comprehension of the repertoire and potential information content of feral cat calls can provide both better understanding of the domestication and socialization process, and improved welfare for feral cats undergoing adoption. Previous studies have used conflicting classification schemes for cat vocalizations, often relying on onomatopoeic or popular descriptions of call types (e.g., "miow"). We studied the vocalizations of 13 unaltered domestic cats that complied with our behavioral definition used to distinguish feral cats from domestic. A total of 71 acoustic units were extracted and visually analyzed for the construction of a hierarchical classification of vocal sounds, based on acoustic properties. We identified 3 major categories (tonal, pulse, and broadband) that further breakdown into 8 subcategories, and show a high degree of reliability when sounds are classified blindly by independent observers (Fleiss' Kappa K = 0.863). Due to the limited behavioral contexts in this study, additional subcategories of cat vocalizations may be identified in the future, but our hierarchical classification system allows for the addition of new categories and new subcategories as they are described. This study shows that cat vocalizations are diverse and complex, and provides an objective and reliable classification system that can be used in future studies.

Disentangling canid howls across multiple species and subspecies: Structure in a complex communication channel.

Wolves, coyotes, and other canids are members of a diverse genus of top predators of considerable conservation and management interest. Canid howls are long-range communication signals, used both for territorial defence and group cohesion. Previous studies have shown that howls can encode individual and group identity. However, no comprehensive study has investigated the nature of variation in canid howls across the wide range of species. We analysed a database of over 2000 howls recorded from 13 different canid species and subspecies. We applied a quantitative similarity measure to compare the modulation pattern in howls from different populations, and then applied an unsupervised clustering algorithm to group the howls into natural units of distinct howl types. We found that different species and subspecies showed markedly different use of howl types, indicating that howl modulation is not arbitrary, but can be used to distinguish one population from another. We give an example of the conservation importance of these findings by comparing the howls of the critically endangered red wolves to those of sympatric coyotes Canis latrans, with whom red wolves may hybridise, potentially compromising reintroduced red wolf populations. We believe that quantitative cross-species comparisons such as these can provide important understanding of the nature and use of communication in socially cooperative species, as well as support conservation and management of wolf populations.

Acoustic sequences in non-human animals: a tutorial review and prospectus.

Animal acoustic communication often takes the form of complex sequences, made up of multiple distinct acoustic units. Apart from the well-known example of birdsong, other animals such as insects, amphibians, and mammals (including bats, rodents, primates, and cetaceans) also generate complex acoustic sequences. Occasionally, such as with birdsong, the adaptive role of these sequences seems clear (e.g. mate attraction and territorial defence). More often however, researchers have only begun to characterise - let alone understand - the significance and meaning of acoustic sequences. Hypotheses abound, but there is little agreement as to how sequences should be defined and analysed. Our review aims to outline suitable methods for testing these hypotheses, and to describe the major limitations to our current and near-future knowledge on questions of acoustic sequences. This review and prospectus is the result of a collaborative effort between 43 scientists from the fields of animal behaviour, ecology and evolution, signal processing, machine learning, quantitative linguistics, and information theory, who gathered for a 2013 workshop entitled, 'Analysing vocal sequences in animals'. Our goal is to present not just a review of the state of the art, but to propose a methodological framework that summarises what we suggest are the best practices for research in this field, across taxa and across disciplines. We also provide a tutorial-style introduction to some of the most promising algorithmic approaches for analysing sequences. We divide our review into three sections: identifying the distinct units of an acoustic sequence, describing the different ways that information can be contained within a sequence, and analysing the structure of that sequence. Each of these sections is further subdivided to address the key questions and approaches in that area. We propose a uniform, systematic, and comprehensive approach to studying sequences, with the goal of clarifying research terms used in different fields, and facilitating collaboration and comparative studies. Allowing greater interdisciplinary collaboration will facilitate the investigation of many important questions in the evolution of communication and sociality.

Estimating vocal repertoire size is like collecting coupons: a theoretical framework with heterogeneity in signal abundance.

Vocal repertoire size is an important behavioural measure in songbirds and mammals with complex vocal communication systems, and has traditionally been used as an indicator of individual fitness, cognitive ability, and social structure. Estimates of asymptotic repertoire size have typically been made using curve fitting techniques. However, the exponential model usually applied in these techniques has never been provided with a theoretical justification based on probability theory, and the model has led to inaccurate estimates. We derived the precise expression for the expected number of distinct signal types observed for a fixed sampling effort: a variation of what is known in the statistical literature as the "Coupon Collector׳s problem". We used empirical data from three species (northern mockingbird, Carolina chickadee, and rock hyrax) to assess the performance of the Coupon Collector model compared to commonly used techniques, such as exponential fitting and repertoire enumeration, and also tested the different models against simulated artificial data sets with the statistical properties of the empirical data. We found that when signal probabilities are dissimilar, the Coupon Collector model provides far more accurate estimates of repertoire size than traditional techniques. Enumeration and exponential curve fitting greatly underestimated repertoire size, despite appearing to have reached saturation. Application of the Coupon Collector model can generate more accurate estimates of repertoire size than the commonly used exponential model of repertoire discovery, and could go a long way towards re-establishing repertoire size as a useful indicator in animal communication research.

Animal vocal sequences: not the Markov chains we thought they were.

Many animals produce vocal sequences that appear complex. Most researchers assume that these sequences are well characterized as Markov chains (i.e. that the probability of a particular vocal element can be calculated from the history of only a finite number of preceding elements). However, this assumption has never been explicitly tested. Furthermore, it is unclear how language could evolve in a single step from a Markovian origin, as is frequently assumed, as no intermediate forms have been found between animal communication and human language. Here, we assess whether animal taxa produce vocal sequences that are better described by Markov chains, or by non-Markovian dynamics such as the 'renewal process' (RP), characterized by a strong tendency to repeat elements. We examined vocal sequences of seven taxa: Bengalese finches Lonchura striata domestica, Carolina chickadees Poecile carolinensis, free-tailed bats Tadarida brasiliensis, rock hyraxes Procavia capensis, pilot whales Globicephala macrorhynchus, killer whales Orcinus orca and orangutans Pongo spp. The vocal systems of most of these species are more consistent with a non-Markovian RP than with the Markovian models traditionally assumed. Our data suggest that non-Markovian vocal sequences may be more common than Markov sequences, which must be taken into account when evaluating alternative hypotheses for the evolution of signalling complexity, and perhaps human language origins.

Landscape influences on dispersal behaviour: a theoretical model and empirical test using the fire salamander, Salamandra infraimmaculata.

When populations reside within a heterogeneous landscape, isolation by distance may not be a good predictor of genetic divergence if dispersal behaviour and therefore gene flow depend on landscape features. Commonly used approaches linking landscape features to gene flow include the least cost path (LCP), random walk (RW), and isolation by resistance (IBR) models. However, none of these models is likely to be the most appropriate for all species and in all environments. We compared the performance of LCP, RW and IBR models of dispersal with the aid of simulations conducted on artificially generated landscapes. We also applied each model to empirical data on the landscape genetics of the endangered fire salamander, Salamandra infraimmaculata, in northern Israel, where conservation planning requires an understanding of the dispersal corridors. Our simulations demonstrate that wide dispersal corridors of the low-cost environment facilitate dispersal in the IBR model, but inhibit dispersal in the RW model. In our empirical study, IBR explained the genetic divergence better than the LCP and RW models (partial Mantel correlation 0.413 for IBR, compared to 0.212 for LCP, and 0.340 for RW). Overall dispersal cost in salamanders was also well predicted by landscape feature slope steepness (76%), and elevation (24%). We conclude that fire salamander dispersal is well characterised by IBR predictions. Together with our simulation findings, these results indicate that wide dispersal corridors facilitate, rather than hinder, salamander dispersal. Comparison of genetic data to dispersal model outputs can be a useful technique in inferring dispersal behaviour from population genetic data.

The encoding of individual identity in dolphin signature whistles: how much information is needed?

Bottlenose dolphins (Tursiops truncatus) produce many vocalisations, including whistles that are unique to the individual producing them. Such "signature whistles" play a role in individual recognition and maintaining group integrity. Previous work has shown that humans can successfully group the spectrographic representations of signature whistles according to the individual dolphins that produced them. However, attempts at using mathematical algorithms to perform a similar task have been less successful. A greater understanding of the encoding of identity information in signature whistles is important for assessing similarity of whistles and thus social influences on the development of these learned calls. We re-examined 400 signature whistles from 20 individual dolphins used in a previous study, and tested the performance of new mathematical algorithms. We compared the measure used in the original study (correlation matrix of evenly sampled frequency measurements) to one used in several previous studies (similarity matrix of time-warped whistles), and to a new algorithm based on the Parsons code, used in music retrieval databases. The Parsons code records the direction of frequency change at each time step, and is effective at capturing human perception of music. We analysed similarity matrices from each of these three techniques, as well as a random control, by unsupervised clustering using three separate techniques: k-means clustering, hierarchical clustering, and an adaptive resonance theory neural network. For each of the three clustering techniques, a seven-level Parsons algorithm provided better clustering than the correlation and dynamic time warping algorithms, and was closer to the near-perfect visual categorisations of human judges. Thus, the Parsons code captures much of the individual identity information present in signature whistles, and may prove useful in studies requiring quantification of whistle similarity.

An image processing based paradigm for the extraction of tonal sounds in cetacean communications.

Dolphins and whales use tonal whistles for communication, and it is known that frequency modulation encodes contextual information. An automated mathematical algorithm could characterize the frequency modulation of tonal calls for use with clustering and classification. Most automatic cetacean whistle processing techniques are based on peak or edge detection or require analyst assistance in verifying detections. An alternative paradigm is introduced using techniques of image processing. Frequency information is extracted as ridges in whistle spectrograms. Spectral ridges are the fundamental structure of tonal vocalizations, and ridge detection is a well-established image processing technique, easily applied to vocalization spectrograms. This paradigm is implemented as freely available matlab scripts, coined IPRiT (image processing ridge tracker). Its fidelity in the reconstruction of synthesized whistles is compared to another published whistle detection software package, silbido. Both algorithms are also applied to real-world recordings of bottlenose dolphin (Tursiops trunactus) signature whistles and tested for the ability to identify whistles belonging to different individuals. IPRiT gave higher fidelity and lower false detection than silbido with synthesized whistles, and reconstructed dolphin identity groups from signature whistles, whereas silbido could not. IPRiT appears to be superior to silbido for the extraction of the precise frequency variation of the whistle.

A global model of malaria climate sensitivity: comparing malaria response to historic climate data based on simulation and officially reported malaria incidence.

BACKGROUND: The role of the Anopheles vector in malaria transmission and the effect of climate on Anopheles populations are well established. Models of the impact of climate change on the global malaria burden now have access to high-resolution climate data, but malaria surveillance data tends to be less precise, making model calibration problematic. Measurement of malaria response to fluctuations in climate variables offers a way to address these difficulties. Given the demonstrated sensitivity of malaria transmission to vector capacity, this work tests response functions to fluctuations in land surface temperature and precipitation. METHODS: This study of regional sensitivity of malaria incidence to year-to-year climate variations used an extended Macdonald Ross compartmental disease model (to compute malaria incidence) built on top of a global Anopheles vector capacity model (based on 10 years of satellite climate data). The predicted incidence was compared with estimates from the World Health Organization and the Malaria Atlas. The models and denominator data used are freely available through the Eclipse Foundation's Spatiotemporal Epidemiological Modeller (STEM). RESULTS: Although the absolute scale factor relating reported malaria to absolute incidence is uncertain, there is a positive correlation between predicted and reported year-to-year variation in malaria burden with an averaged root mean square (RMS) error of 25% comparing normalized incidence across 86 countries. Based on this, the proposed measure of sensitivity of malaria to variations in climate variables indicates locations where malaria is most likely to increase or decrease in response to specific climate factors. Bootstrapping measures the increased uncertainty in predicting malaria sensitivity when reporting is restricted to national level and an annual basis. Results indicate a potential 20x improvement in accuracy if data were available at the level ISO 3166-2 national subdivisions and with monthly time sampling. CONCLUSIONS: The high spatial resolution possible with state-of-the-art numerical models can identify regions most likely to require intervention due to climate changes. Higher-resolution surveillance data can provide a better understanding of how climate fluctuations affect malaria incidence and improve predictions. An open-source modelling framework, such as STEM, can be a valuable tool for the scientific community and provide a collaborative platform for developing such models.

Modelling transmission of vector-borne pathogens shows complex dynamics when vector feeding sites are limited.

The relationship between species richness and the prevalence of vector-borne disease has been widely studied with a range of outcomes. Increasing the number of host species for a pathogen may decrease infection prevalence (dilution effect), increase it (amplification), or have no effect. We derive a general model, and a specific implementation, which show that when the number of vector feeding sites on each host is limiting, the effects on pathogen dynamics of host population size are more complex than previously thought. The model examines vector-borne disease in the presence of different host species that are either competent or incompetent (i.e. that cannot transmit the pathogen to vectors) as reservoirs for the pathogen. With a single host species present, the basic reproduction ratio R(0) is a non-monotonic function of the population size of host individuals (H), i.e. a value [Formula: see text] exists that maximises R(0). Surprisingly, if [Formula: see text] a reduction in host population size may actually increase R(0). Extending this model to a two-host species system, incompetent individuals from the second host species can alter the value of [Formula: see text] which may reverse the effect on pathogen prevalence of host population reduction. We argue that when vector-feeding sites on hosts are limiting, the net effect of increasing host diversity might not be correctly predicted using simple frequency-dependent epidemiological models.

Syntactic structure and geographical dialects in the songs of male rock hyraxes.

Few mammalian species produce vocalizations that are as richly structured as bird songs, and this greatly restricts the capacity for information transfer. Syntactically complex mammalian vocalizations have been previously studied only in primates, cetaceans and bats. We provide evidence of complex syntactic vocalizations in a small social mammal: the rock hyrax (Procavia capensis: Hyracoidea). We adopted three algorithms, commonly used in genetic sequence analysis and information theory, to examine the order of syllables in hyrax calls. Syntactic dialects exist, and the syntax of hyrax calls is significantly different between different regions in Israel. Call syntax difference is positively correlated to geographical distance over short distances. No correlation is found over long distances, which may reflect limited dispersal movement. These findings indicate that rich syntactic structure is more common in the vocalizations of mammalian taxa than previously thought and suggest the possibility of vocal production learning in the hyrax.

Unraveling seasonality in population averages: an examination of seasonal variation in glucose levels in diabetes patients using a large population-based data set.

It has been shown that the population average blood glucose level of diabetes patients shows seasonal variation, with higher levels in the winter than summer. However, seasonality in the population averages could be due to a tendency in the individual to seasonal variation, or alternatively due to occasional high winter readings (spiking), with different individuals showing this increase in different winters. A method was developed to rule out spiking as the dominant pattern underlying the seasonal variation in the population averages. Three years of data from three community-serving laboratories in Israel were retrieved. Diabetes patients (N = 3243) with a blood glucose result every winter and summer over the study period were selected. For each individual, the following were calculated: seasonal average glucose for all winters and summers over the period of study (2006-2009), winter-summer difference for each adjacent winter-summer pair, and average of these five differences, an index of the degree of spikiness in the pattern of the six seasonal levels, and number of times out of five that each winter-summer difference was positive. Seasonal population averages were examined. The distribution of the individual's differences between adjacent seasons (winter minus summer) was examined and compared between subgroups. Seasonal population averages were reexamined in groups divided according to the index of the degree of spikiness in the individual's glucose pattern over the series of seasons. Seasonal population averages showed higher winter than summer levels. The overall median winter-summer difference on the individual level was 8 mg/dL (0.4 mmol/L). In 16.9% (95% confidence interval [CI]: 15.6-18.2%) of the population, all five winter-summer differences were positive versus 3.6% (95% CI: 3.0-4.2%) where all five winter-summer differences were negative. Seasonal variation in the population averages was not attenuated in the group having the lowest spikiness index; comparison of the distributions of the winter-summer differences in the high-, medium-, and low-spikiness groups showed no significant difference (p = .213). Therefore, seasonality in the population average blood glucose in diabetes patients is not just the result of occasional high measurements in different individuals in different winters, but presumably reflects a general periodic tendency in individuals for winter glucose levels to be higher than summer levels.