Behavioral Ecology Research Articles

Odorant-binding proteins in canine anal sac glands indicate an evolutionarily conserved role in mammalian chemical communication

BackgroundChemical communication is an important aspect of the behavioural ecology of a wide range of mammals. In dogs and other carnivores, anal sac glands are thought to convey information to conspecifics by secreting a pallet of small volatile molecules produced by symbiotic bacteria. Because these glands are unique to carnivores, it is unclear how their secretions relate to those of other placental mammals that make use of different tissues and secretions for chemical communication. Here we analyse the anal sac glands of domestic dogs to verify the secretion of proteins and infer their evolutionary relationship to those involved in the chemical communication of non-carnivoran mammals.ResultsProteomic analysis of anal sac gland secretions of 17 dogs revealed the consistently abundant presence of three related proteins. Homology searches against online databases indicate that these proteins are evolutionary related to ‘odorant binding proteins’ (OBPs) found in a wide range of mammalian secretions and known to contribute to chemical communication. Screening of the dog’s genome sequence show that the newly discovered OBPs are encoded by a single cluster of three genes in the pseudoautosomal region of the X-chromosome. Comparative genomic screening indicates that the same locus is shared by a wide range of placental mammals and that it originated at least before the radiation of extant placental orders. Phylogenetic analyses suggest a dynamic evolution of gene duplication and loss, resulting in large gene clusters in some placental taxa and recurrent loss of this locus in others. The homology of OBPs in canid anal sac glands and those found in other mammalian secretions implies that these proteins maintained a function in chemical communication throughout mammalian evolutionary history by multiple shifts in expression between secretory tissues involved in signal release and nasal mucosa involved in signal reception.ConclusionsOur study elucidates a poorly understood part of the biology of a species that lives in close association with humans. In addition, it shows that the protein repertoire underlying chemical communication in mammals is more evolutionarily stable than the variation of involved glands and tissues would suggest.

Functional and ecological correlates of the primate jaw abductors.

While the adductor musculature of the primate jaw has been extensively analyzed within the context of dietary and social ecology, little is known about the corresponding muscles of jaw abduction. Nonetheless, these muscles significantly contribute to a species' maximum gape potential, and thus might constrain dietary niche diversity and impact social display behaviors. In this study, we quantify the architectural properties of the digastric (a jaw abductor) and lateral pterygoid (a jaw abductor and anterior translator) across a broad sample of male and female anthropoid primates. We test the hypothesis that the abductor musculature reflects specialization to dietary and behavioral ecology. Our sample comprises 14 catarrhine and 13 platyrrhine species spanning a wide range of dietary and social categories. All specimens were sharp dissected and muscles subsequently chemically digested using a standardized protocol. Our findings demonstrate that relative fascicle lengths within the lateral pterygoid (but not the digastric) are significantly greater within species that habitually consume larger food items. Meanwhile, canine length is more strongly associated with fascicle lengths in the digastric than in the lateral pterygoid, particularly within males. Neither dietary mechanical resistance nor the intensity of social competition relates to the size or architectural properties of the jaw abductors. These findings suggest that dietary-and to a lesser extent, socioecological-aspects of a primate's life history may be reflected in the architecture of these muscles, albeit to varying degrees. This underlines the importance of considering the complete masticatory apparatus when interpreting the evolution of the primate jaw.

Living in tiny fragments: a glimpse at the ecology of Goodman's mouse lemurs (Microcebus lehilahytsara) in the relic forest of Ankafobe, Central Highlands, Madagascar.

Habitat fragmentation is one of the major types of anthropogenic change, though fragmented landscapes predate human intervention. At present, the Central Highlands of Madagascar are covered by extensive grasslands interspersed with small discrete forest patches of unknown antiquity. Ankafobe, an actively protected site, comprises two such fragments of 12 and 30ha, respectively, known to harbor three lemur species and other endemic wildlife. At this location, we conducted a survey of resident Goodman's mouse lemurs, Microcebus lehilahytsara, to determine baseline behavioral and ecological conditions for this isolated population. By studying primates in forest fragments, investigators can characterize the effects of shrinking habitats and decreasing connectivity on species diversity and survival, thus providing a glimpse into the potential resilience of species in the face of anthropogenic disturbance. Investigating the behavioral ecology of Goodman's mouse lemurs across their geographic range could help us understand their metabolic and ecological flexibility and predict species long-term survival prospects. We conducted night transect walks, using capture techniques and telemetry, to track eight radio-collared individuals. Preliminary density estimates based on a limited number of sightings (n = 18) were 2.19ind/ha, and home range assessments ranged between 0.22 and 3.67ha. Mouse lemurs traveled an average of 425m nightly during the 5-h tracking periods and primarily fed on fruits of the mistletoe Bakerella clavata. The finding that Goodman's mouse lemurs apparently thrive in the seasonally cold and arid forest fragments in the Central Highlands indicates that they may be among the most tolerant and adaptable lemur species in Madagascar. These results point towards an exciting research program that focuses on ecological tolerance as a mechanism for long-term species survival.

Tribute for James (Jim) E Wright

Jim was born in Maryland in 1936, and passed away at his home near Hebden Bridge on 28th February, 2020. He was a member of academic staff in Psychology at the University of Leeds for over 30 years; his huge impact on academic colleagues and students, arising from his passionate interest in the discipline of Psychology, and from his ability to engage and inspire other people – that is his gift to the field. Jim’s academic influence can be seen in three areas: his almost single-handed facilitation of Behaviour Analysis in the UK in the 1970s and 80s; his work supporting field observations in behavioural ecology; and his work on schedules of reinforcement. More important than these scholarly achievements, Jim was admired and respected by the whole Psychological community as a warm, positive, and generous human being. He brought joy to the Leeds Department and to the UK learning community. Jim represented the best in human values, and he was loved by everyone. Without his influence many of today’s learning theorists would not be learning theorists.

The role of great ape behavioral ecology in One Health: Implications for captive welfare and re-habilitation success.

Behavior is the interface through which animals interact with their environments, and therefore has potentially cascading impacts on the health of individuals, populations, their habitats, and the humans that share them. Evolution has shaped the interaction between species and their environments. Thus, alterations to the species-typical "wild-type" behavioral repertoire (and the ability of the individual to adapt flexibly which elements of the repertoire it employs) may disrupt the relationship between the organism and its environment, creating cascading One Health effects. A good example is rehabilitant orangutans where, for example, seemingly minor differences from wild conspecifics in the time spent traveling on the ground rather than in the forest canopy can affect an individual's musculoskeletal and nutritional health, as well as social integration. It can also increase two-way transmission of infectious diseases and/or pathogens with local human populations, or potentially with neighboring wild populations if there are no geographical barriers and rehabilitants travel far enough to leave their release area. Primates are well known ecosystem engineers, reshaping plant communities and maintaining biodiversity through seed dispersal, consuming plants, and creating canopy gaps and trails. From the habitat perspective, a rehabilitant orangutan which does not behave like a wild orangutan is unlikely to fulfill these same ecosystem services. Despite the importance of the diversity of an ape's behavioral repertoire, how it compares to that of wild conspecifics and how it alters in response to habitat variation, behavior is an often under-appreciated aspect of One Health. In this review, focusing on orangutans as an example of the kinds of problems faced by all captive great apes, we examine the ways in which understanding and facilitating the expression of wild-type behavior can improve their health, their ability to thrive, and the robustness of local One Health systems.

The behavioural ecology behind anti-predator mechanisms: diversity, ontogenetic changes and sexual differences in anuran defence behaviours

Anti-predator mechanisms play a key role in the survival of any animal in nature. Anurans exhibit a great diversity of defensive behaviours and interact with the widest range of predators of any vertebrates. However, there are few systematic and experimental studies of anuran defensive behaviours, which are generally opportunistic. Here, we deploy a range of methods to investigate various facets of anuran defensive behaviour using the cane toad Rhinella marina as a model organism. This originally Amazonian anuran is now widely distributed across the globe and has caused several predators to decline at introduction sites where this species is not native, a direct result of its anti-predation defenses. First, we compiled previously published data on anuran predation events to assess the relationship between predator/anuran size and predator size and type. We then performed a systematic experiment to test the hypothesis that there is an ontogenetic variation in cane toad behavioural defense displays, as well as a variation in these displays between males and females. In total, we tested 173 individuals including juveniles, adult males and adult females. We show that the size and type of the predator is related to the size of the anuran as prey and that this, in turn, has led to the adoption of different predation-avoiding behavioural defensive strategies during ontogeny. Our results also indicate that both the sex and the size of anurans influence the adoption of defensive strategies.

The Evolution of Social Behaviour

The Evolution of Social Behaviour

Collaboration enhances career progression in academic science, especially for female researchers.

Collaboration and diversity are increasingly promoted in science. Yet how collaborations influence academic career progression, and whether this differs by gender, remains largely unknown. Here, we use co-authorship ego networks to quantify collaboration behaviour and career progression of a cohort of contributors to biennial International Society of Behavioral Ecology meetings (1992, 1994, 1996). Among this cohort, women were slower and less likely to become a principal investigator (PI; approximated by having at least three last-author publications) and published fewer papers over fewer years (i.e. had shorter academic careers) than men. After adjusting for publication number, women also had fewer collaborators (lower adjusted network size) and published fewer times with each co-author (lower adjusted tie strength), albeit more often with the same group of collaborators (higher adjusted clustering coefficient). Authors with stronger networks were more likely to become a PI, and those with less clustered networks did so more quickly. Women, however, showed a stronger positive relationship with adjusted network size (increased career length) and adjusted tie strength (increased likelihood to become a PI). Finally, early-career network characteristics correlated with career length. Our results suggest that large and varied collaboration networks are positively correlated with career progression, especially for women.

Intraspecific facial bite marks in tyrannosaurids provide insight into sexual maturity and evolution of bird-like intersexual display

AbstractIntraspecific aggression, or agonism, is a widespread intrasexual selective behavior important to understanding animal behavioral ecology and reproductive systems. Such behavior can be studied either by direct observation or inferred from wound/scar frequency in extant species but is difficult to document in extinct taxa, limiting understanding of its evolution. Among extant archosaurs, crocodylians display extensive intrasexual aggression, whereas birds show extreme visual/vocal intersexual display. The evolutionary origin of this behavioral divergence, and pattern in non-avian dinosaurs, is unknown. Here we document the morphology, frequency, and ontogeny of intraspecific facial bite lesions (324 lesions) in a large sample of tyrannosaurids (202 specimens, 528 elements) to infer patterns of intraspecific aggression in non-avian theropods. Facial scars are consistent in position and orientation across tyrannosaurid species, suggesting bites were inflicted due to repeated/postured behavior. Facial scars are absent in young tyrannosaurids, first appear in immature animals (~50% adult skull length), are present in ~60% of the adult-sized specimens, and show aggressor:victim size isometry. The ontogenetic distribution of bite scars suggests agonistic behavior is associated with the onset of sexual maturity, and scar presence in approximately half the specimens may relate to a sexual pattern. Considered in a phylogenetic context, intraspecific bite marks are consistent and widely distributed in fossil and extant crocodyliforms and non-maniraptoriform theropods, suggesting a potential plesiomorphic behavior in archosaurs. Their absence in maniraptoriform theropods, including birds, may reflect a transition from boney cranial ornamentation and crocodylian-like intrasexual aggression to avian-like intersexual display with the evolution of pennaceous feathers.

Implementing social network analysis to understand the socioecology of wildlife co-occurrence and joint interactions with humans in anthropogenic environments.

Human population expansion into wildlife habitats has increased interest in the behavioural ecology of human-wildlife interactions. To date, however, the socioecological factors that determine whether, when or where wild animals take risks by interacting with humans and anthropogenic factors still remains unclear. We adopt a comparative approach to address this gap, using social network analysis (SNA). SNA, increasingly implemented to determine human impact on wildlife ecology, can be a powerful tool to understand how animal socioecology influences the spatiotemporal distribution of human-wildlife interactions. For 10 groups of rhesus, long-tailed and bonnet macaques (Macaca spp.) living in anthropogenically impacted environments in Asia, we collected data on human-macaque interactions, animal demographics, and macaque-macaque agonistic and affiliative social interactions. We constructed 'human co-interaction networks' based on associations between macaques that interacted with humans within the same time and spatial locations, and social networks based on macaque-macaque allogrooming behaviour, affiliative behaviours of short duration (agonistic support, lip-smacking, silent bare-teeth displays and non-sexual mounting) and proximity. Pre-network permutation tests revealed that, within all macaque groups, specific individuals jointly took risks by repeatedly, consistently co-interacting with humans within and across time and space. GLMMs revealed that macaques' tendencies to co-interact with humans was positively predicted by their tendencies to engage in short-duration affiliative interactions and tolerance of conspecifics, although the latter varied across species (bonnets>rhesus>long-tailed). Male macaques were more likely to co-interact with humans than females. Neither macaques' grooming relationships nor their dominance ranks predicted their tendencies to co-interact with humans. Our findings suggest that, in challenging anthropogenic environments, less (compared to more) time-consuming forms of affiliation, and additionally greater social tolerance in less ecologically flexible species with a shorter history of exposure to humans, may be key to animals' joint propensities to take risks to gain access to resources. For males, greater exploratory tendencies and less energetically demanding long-term life-history strategies (compared to females) may also influence such joint risk-taking. From conservation and public health perspectives, wildlife connectedness within such co-interaction networks may inform interventions to mitigate zoonosis, and move human-wildlife interactions from conflict towards coexistence.

Impact of extreme environmental conditions: Foraging behaviour and trophic ecology responses of a diving seabird, the common diving petrel

The reproductive success of birds is strongly driven by environmental conditions at different time scales. Thus, during periods of low food availability, breeding success is constrained by the ability of adults to adapt their foraging effort and feeding behaviour to maintain regular incubation shifts and chick provisioning. However, while large seabirds can buffer disruptions in prey availability, the ecophysiological constraints of smaller species may limit their behavioural flexibility. By combining information on at-sea movements, foraging habitat, trophic niche, and breeding success, this study evaluated the effects of intense variability in oceanographic conditions on common diving petrels (Pelecanoides urinatrix) at the northern extent of their range in south-eastern Australia during four consecutive breeding seasons. Unusually low breeding success (6 and 0%) was observed during two years with intense heatwave events, which were associated with higher foraging effort (foraging trips twice longer) and a substantial shift in trophic niche (lower blood δ15N values). These findings suggest that common diving petrels in Bass Strait may have reached a critical threshold above which buffering the effects of environmental variability on their reproductive output is not possible. The clear cascading impacts that marine heatwaves have on zooplankton feeders illustrate the profound bottom-up effect induced by such extreme environmental variations, and suggest strong impact on higher-trophic levels. The wide, circumpolar breeding distribution of the common diving petrel, and its high sensitivity to variations in oceanographic conditions, suggest that this species may be a suitable model to study short-term and long-term behavioural responses to the effects of climate change throughout the Southern Ocean.

Estimating the reproducibility of social learning research published between 1955 and 2018.

Reproducibility is integral to science, but difficult to achieve. Previous research has quantified low rates of data availability and results reproducibility across the biological and behavioural sciences. Here, we surveyed 560 empirical publications, published between 1955 and 2018 in the social learning literature, a research topic that spans animal behaviour, behavioural ecology, cultural evolution and evolutionary psychology. Data were recoverable online or through direct data requests for 30% of this sample. Data recovery declines exponentially with time since publication, halving every 6 years, and up to every 9 years for human experimental data. When data for a publication can be recovered, we estimate a high probability of subsequent data usability (87%), analytical clarity (97%) and agreement of published results with reproduced findings (96%). This corresponds to an overall rate of recovering data and reproducing results of 23%, largely driven by the unavailability or incompleteness of data. We thus outline clear measures to improve the reproducibility of research on the ecology and evolution of social behaviour.

Time-Activity Budget of the Snowy Sheathbill (Chionis albus) Wintering at a Sea Lion (Otaria flavescens) Haul-Out in Argentina

This work aims to provide information regarding the behavioral ecology of the least studied of the two sheathbill species, the Snowy Sheathbill (Chionis albus), wintering in northern Argentina in a male South American Sea Lion (Otaria flavescens) haul-out. Data about bird abundances and time allocated to behaviors was gathered during the final stage of three consecutive non-breeding seasons. Significant differences were found in the abundance between and within seasons. Overall, sheathbills allocated most of their time to foraging, followed by resting and self-maintaining, with the least of the time allocated to agonistic behaviors. The results obtained by the authors demonstrated that the Snowy Sheathbill recurrently used the local sea-lion haul-out as a foraging ground, with steady numbers throughout the non-breeding seasons.

Vertebrate prey capture by Latrodectus mactans (Walckenaer, 1805) and Steatoda triangulosa (Walckenaer, 1802) (Araneae, Theridiidae) provide further insights into the immobilization and hoisting mechanisms of large prey

Spider species across 27 families have been recorded naturally preying upon vertebrates. Intricate three-dimensional webs, predation strategies, and potent neurotoxic venom allow Latrodectus and Steatoda spiders to subdue vertebrate prey that are many times larger and heavier than themselves. Yet, little is known about the behaviour associated with capturing comparatively large vertebrate prey, or how common these predatory events are. We report on two new cases of vertebrate predation by Latrodectinae spiders: a Latrodectus mactans (Walckenaer, 1805) preying on a common house mouse Mus musculus (Linnaeus, 1758) in the USA and a Steatoda triangulosa (Walckenaer, 1802) preying on a Kotschy's gecko Mediodactylus kotschyi (Steindachner, 1870) in Greece. Although predation events on vertebrates by Latrodectus species have been documented in the literature, such events have been sparsely reported for the genus Steatoda. We provide the first record of S. triangulosa preying on M. kotschyi. Such predation events shed light on the multifunctional physiology of the venom and behavioural ecology of these spiders.

A relative‐motion method for parsing spatiotemporal behaviour of dyads using GPS relocation data

Abstract In this paper, we introduce a novel method for classifying and computing the frequencies of movement modes of intraspecific and interspecific dyads, focusing in particular on distance‐mediated approach, retreat, following and side‐by‐side movement modes. Besides distance, other factors such as time of day, season, sex or age can be included in the analysis to assess whether they cause frequencies of movement modes to deviate from random. By subdividing the data according to selected factors, our method allows us to identify those responsible for (or correlated with) significant differences in the behaviour of dyadic pairs. We demonstrate and validate our method using both simulated and empirical data. Our simulated data were obtained from a relative‐motion, biased random‐walk (RM‐BRW) model with attraction and repulsion components. Our empirical data were GPS relocation data collected from African elephants in Etosha National Park, Namibia. The simulated data were primarily used to validate our method while the empirical data were used to illustrate the types of behavioural assessment that our methodology reveals. Our method facilitates automated, observer‐bias‐free analysis of the locomotive interactions of dyads using GPS relocation data, which are becoming increasingly ubiquitous as telemetry and related technologies improve. It should open up a whole new vista of behavioural‐interaction type analyses to movement and behavioural ecologists.

Where Do Online Games Fit into the Health Behaviour Ecology of Emerging Adults: A Scoping Review.

Online video games are a common pastime for emerging adults (EAs). EAs are an age group that is of interest in health communication because habits formed during this life stage can cause or prevent disease later in life. Guided by three research questions, this scoping review identifies the current state of research into socio-ecological influences on physical activity and diet behaviours of EAs. The review also examines the role that online video games play within this behavioural ecology. In total, 112 articles were found that focused on behavioural ecological influences for physical activity and diet behaviour among EAs. Seven of these articles focused on the impact of online video games, although only in conjunction with their influence on physical activity, identifying a gap in understanding the influence of online games on diet. Results show that online video games are currently under-researched in terms of impacts on physical activity and diet despite the prevalence of the use of these games within the EA cohort.

An ecological approach to measuring synchronization abilities across the animal kingdom.

In this perspective paper, we focus on the study of synchronization abilities across the animal kingdom. We propose an ecological approach to studying nonhuman animal synchronization that begins from observations about when, how and why an animal might synchronize spontaneously with natural environmental rhythms. We discuss what we consider to be the most important, but thus far largely understudied, temporal, physical, perceptual and motivational constraints that must be taken into account when designing experiments to test synchronization in nonhuman animals. First and foremost, different species are likely to be sensitive to and therefore capable of synchronizing at different timescales. We also argue that it is fruitful to consider the latent flexibility of animal synchronization. Finally, we discuss the importance of an animal's motivational state for showcasing synchronization abilities. We demonstrate that the likelihood that an animal can successfully synchronize with an environmental rhythm is context-dependent and suggest that the list of species capable of synchronization is likely to grow when tested with ecologically honest, species-tuned experiments.This article is part of the theme issue ‘Synchrony and rhythm interaction: from the brain to behavioural ecology’.

Rhythm interaction in animal groups: selective attention in communication networks.

Animals communicating interactively with conspecifics often time their broadcasts to avoid overlapping interference, to emit leading, as opposed to following, signals or to synchronize their signalling rhythms. Each of these adjustments becomes more difficult as the number of interactants increases beyond a pair. Among acoustic species, insects and anurans generally deal with the problem of group signalling by means of 'selective attention' in which they focus on several close or conspicuous neighbours and ignore the rest. In these animals, where signalling and receiving are often dictated by sex, the process of selective attention in signallers may have a parallel counterpart in receivers, which also focus on close neighbours. In birds and mammals, local groups tend to be extended families or clans, and group signalling may entail complex timing mechanisms that allow for attention to all individuals. In general, the mechanisms that allow animals to communicate in groups appear to be fully interwoven with the basic process of rhythmic signalling. This article is part of the theme issue 'Synchrony and rhythm interaction: from the brain to behavioural ecology'.

Extreme precision in rhythmic interaction is enabled by role-optimized sensorimotor coupling: analysis and modelling of West African drum ensemble music.

Human social interactions often involve carefully synchronized behaviours. Musical performance in particular features precise timing and depends on the differentiation and coordination of musical/social roles. Here, we study the influence of musical/social roles, individual musicians and different ensembles on rhythmic synchronization in Malian drum ensemble music, which features synchronization accuracy near the limits of human performance. We analysed 72 recordings of the same piece performed by four trios, in which two drummers in each trio systematically switched roles (lead versus accompaniment). Musical role, rather than individual or group differences, is the main factor influencing synchronization accuracy. Using linear causal modelling, we found a consistent pattern of bi-directional couplings between players, in which the direction and strength of rhythmic adaptation is asymmetrically distributed across musical roles. This differs from notions of musical leadership, which assume that ensemble synchronization relies predominantly on a single dominant personality and/or musical role. We then ran simulations that varied the direction and strength of sensorimotor coupling and found that the coupling pattern used by the Malian musicians affords nearly optimal synchronization. More broadly, our study showcases the importance of ecologically valid and culturally diverse studies of human behaviour.This article is part of the theme issue ‘Synchrony and rhythm interaction: from the brain to behavioural ecology’.

Vocal learning as a preadaptation for the evolution of human beat perception and synchronization.

The human capacity to synchronize movements to an auditory beat is central to musical behaviour and to debates over the evolution of human musicality. Have humans evolved any neural specializations for music processing, or does music rely entirely on brain circuits that evolved for other reasons? The vocal learning and rhythmic synchronization hypothesis proposes that our ability to move in time with an auditory beat in a precise, predictive and tempo-flexible manner originated in the neural circuitry for complex vocal learning. In the 15 years since the hypothesis was proposed a variety of studies have supported it. However, one study has provided a significant challenge to the hypothesis. Furthermore, it is increasingly clear that vocal learning is not a binary trait animals have or lack, but varies more continuously across species. In the light of these developments and of recent progress in the neurobiology of beat processing and of vocal learning, the current paper revises the vocal learning hypothesis. It argues that an advanced form of vocal learning acts as a preadaptation for sporadic beat perception and synchronization (BPS), providing intrinsic rewards for predicting the temporal structure of complex acoustic sequences. It further proposes that in humans, mechanisms of gene-culture coevolution transformed this preadaptation into a genuine neural adaptation for sustained BPS. The larger significance of this proposal is that it outlines a hypothesis of cognitive gene-culture coevolution which makes testable predictions for neuroscience, cross-species studies and genetics.This article is part of the theme issue ‘Synchrony and rhythm interaction: from the brain to behavioural ecology’.