Sensory collectives in natural systems.

Groups of animals inhabit vastly different sensory worlds, or umwelten, which shape fundamental aspects of their behaviour. Yet the sensory ecology of species is rarely incorporated into the emerging field of collective behaviour, which studies the movements, population-level behaviours, and emergent properties of animal groups. Here, we review the contributions of sensory ecology and collective behaviour to understanding how animals move and interact within the context of their social and physical environments. Our goal is to advance and bridge these two areas of inquiry and highlight the potential for their creative integration. To achieve this goal, we organise our review around the following themes: (1) identifying the promise of integrating collective behaviour and sensory ecology; (2) defining and exploring the concept of a 'sensory collective'; (3) considering the potential for sensory collectives to shape the evolution of sensory systems; (4) exploring examples from diverse taxa to illustrate neural circuits involved in sensing and collective behaviour; and (5) suggesting the need for creative conceptual and methodological advances to quantify 'sensescapes'. In the final section, (6) applications to biological conservation, we argue that these topics are timely, given the ongoing anthropogenic changes to sensory stimuli (e.g. via light, sound, and chemical pollution) which are anticipated to impact animal collectives and group-level behaviour and, in turn, ecosystem composition and function. Our synthesis seeks to provide a forward-looking perspective on how sensory ecologists and collective behaviourists can both learn from and inspire one another to advance our understanding of animal behaviour, ecology, adaptation, and evolution.

The behaviour and activity budgets of two sympatric sloths; Bradypus variegatus and Choloepus hoffmanni.

It is usually beneficial for species to restrict activity to a particular phase of the 24-hour cycle as this enables the development of morphological and behavioural adaptations to enhance survival under specific biotic and abiotic conditions. Sloth activity patterns are thought to be strongly related to the environmental conditions due to the metabolic consequences of having a low and highly variable core body temperature. Understanding the drivers of sloth activity and their ability to withstand environmental fluctuations is of growing importance for the development of effective conservation measures, particularly when we consider the vulnerability of tropical ecosystems to climate change and the escalating impacts of anthropogenic activities in South and Central America. Unfortunately, the cryptic nature of sloths makes long term observational research difficult and so there is very little existing literature examining the behavioural ecology of wild sloths. Here, we used micro data loggers to continuously record, for the first time, the behaviour of both Bradypus and Choloepus sloths over periods of days to weeks. We investigate how fluctuations in the environmental conditions affect the activity of sloths inhabiting a lowland rainforest on the Caribbean coast of Costa Rica and examined how this might relate to their low power lifestyle. Both Bradypus and Choloepus sloths were found to be cathemeral in their activity, with high levels of between-individual and within-individual variation in the amounts of time spent active, and in the temporal distribution of activity over the 24-hour cycle. Daily temperature did not affect activity, although Bradypus sloths were found to show increased nocturnal activity on colder nights, and on nights following colder days. Our results demonstrate a distinct lack of synchronicity within the same population, and we suggest that this pattern provides sloths with the flexibility to exploit favourable environmental conditions whilst reducing the threat of predation.

New frontiers in bird migration research.

Bird migrations are impressive behavioral phenomena, representing complex spatiotemporal strategies to balance costs of living while maximizing fitness. The field of bird migration research has made great strides over the past decades, yet fundamental gaps remain. Technologies have sparked a transformation in the study of bird migration research by revealing remarkable insights into the underlying behavioral, cognitive, physiological and evolutionary mechanisms of these diverse journeys. Here, we aim to encourage broad discussions and promote future studies by highlighting research fields that are characterized by major knowledge gaps or conflicting evidence, namely the fields of navigation, social learning, individual development, energetics and conservation. We approach each topic by summarizing the current state of knowledge and provide a future outlook of ideas and state-of-the-art methods to further advance the field. Integrating knowledge across these disciplines will allow us to understand the adaptive abilities of different species and to develop effective conservation strategies in a rapidly changing world.

Individual tracking reveals long-distance flight-path control in a nocturnally migrating moth.

Each year, trillions of insects make long-range seasonal migrations. These movements are relatively well understood at a population level, but how individual insects achieve them remains elusive. Behavioral responses to conditions en route are little studied, primarily owing to the challenges of tracking individual insects. Using a light aircraft and individual radio tracking, we show that nocturnally migrating death's-head hawkmoths maintain control of their flight trajectories over long distances. The moths did not just fly with favorable tailwinds; during a given night, they also adjusted for head and crosswinds to precisely hold course. This behavior indicates that the moths use a sophisticated internal compass to maintain seasonally beneficial migratory trajectories independent of wind conditions, illuminating how insects traverse long distances to take advantage of seasonal resources.

How often should dead-reckoned animal movement paths be corrected for drift?

BACKGROUND: Understanding what animals do in time and space is important for a range of ecological questions, however accurate estimates of how animals use space is challenging. Within the use of animal-attached tags, radio telemetry (including the Global Positioning System, 'GPS') is typically used to verify an animal's location periodically. Straight lines are typically drawn between these 'Verified Positions' ('VPs') so the interpolation of space-use is limited by the temporal and spatial resolution of the system's measurement. As such, parameters such as route-taken and distance travelled can be poorly represented when using VP systems alone. Dead-reckoning has been suggested as a technique to improve the accuracy and resolution of reconstructed movement paths, whilst maximising battery life of VP systems. This typically involves deriving travel vectors from motion sensor systems and periodically correcting path dimensions for drift with simultaneously deployed VP systems. How often paths should be corrected for drift, however, has remained unclear. METHODS AND RESULTS: Here, we review the utility of dead-reckoning across four contrasting model species using different forms of locomotion (the African lion Panthera leo, the red-tailed tropicbird Phaethon rubricauda, the Magellanic penguin Spheniscus magellanicus, and the imperial cormorant Leucocarbo atriceps). Simulations were performed to examine the extent of dead-reckoning error, relative to VPs, as a function of Verified Position correction (VP correction) rate and the effect of this on estimates of distance moved. Dead-reckoning error was greatest for animals travelling within air and water. We demonstrate how sources of measurement error can arise within VP-corrected dead-reckoned tracks and propose advancements to this procedure to maximise dead-reckoning accuracy. CONCLUSIONS: We review the utility of VP-corrected dead-reckoning according to movement type and consider a range of ecological questions that would benefit from dead-reckoning, primarily concerning animal-barrier interactions and foraging strategies.

Quantum simulation of 2D antiferromagnets with hundreds of Rydberg atoms.

Quantum simulation using synthetic systems is a promising route to solve outstanding quantum many-body problems in regimes where other approaches, including numerical ones, fail1. Many platforms are being developed towards this goal, in particular based on trapped ions2-4, superconducting circuits5-7, neutral atoms8-11 or molecules12,13. All of these platforms face two key challenges: scaling up the ensemble size while retaining high-quality control over the parameters, and validating the outputs for these large systems. Here we use programmable arrays of individual atoms trapped in optical tweezers, with interactions controlled by laser excitation to Rydberg states11, to implement an iconic many-body problem-the antiferromagnetic two-dimensional transverse-field Ising model. We push this platform to a regime with up to 196 atoms manipulated with high fidelity and probe the antiferromagnetic order by dynamically tuning the parameters of the Hamiltonian. We illustrate the versatility of our platform by exploring various system sizes on two qualitatively different geometries-square and triangular arrays. We obtain good agreement with numerical calculations up to a computationally feasible size (approximately 100 particles). This work demonstrates that our platform can be readily used to address open questions in many-body physics.

Certainty and integration of options in animal movement.

Physical energy defines the energy landscape and determines the species-specific cost of movement, thus influencing movement decisions. In unpredictable and dynamic environments, observing the locomotion of others increases individual certainty in the distribution of physical energy to increase movement efficiency. Beyond the physical energy landscape, social sampling increases certainty in all ecological landscapes that influence animal movement (including fear and resource landscapes), and individuals use energy to express each of these. We call for the development of an 'optimal movement theory' (OMT) that integrates the multidimensional reality of movement decisions by combining ecological landscapes according to a single expectation of energy cost-benefit, where social sampling provides up-to-date information under uncertain conditions. This mechanistic framework has implications for predicting individual movement patterns and for investigating the emergence of aggregations.

An "orientation sphere" visualization for examining animal head movements.

Animal behavior is elicited, in part, in response to external conditions, but understanding how animals perceive the environment and make the decisions that bring about these behavioral responses is challenging.Animal heads often move during specific behaviors and, additionally, typically have sensory systems (notably vision, smell, and hearing) sampling in defined arcs (normally to the front of their heads). As such, head-mounted electronic sensors consisting of accelerometers and magnetometers, which can be used to determine the movement and directionality of animal heads (where head "movement" is defined here as changes in heading [azimuth] and/or pitch [elevation angle]), can potentially provide information both on behaviors in general and also clarify which parts of the environment the animals might be prioritizing ("environmental framing").We propose a new approach to visualize the data of such head-mounted tags that combines the instantaneous outputs of head heading and pitch in a single intuitive spherical plot. This sphere has magnetic heading denoted by "longitude" position and head pitch by "latitude" on this "orientation sphere" (O-sphere).We construct the O-sphere for the head rotations of a number of vertebrates with contrasting body shape and ecology (oryx, sheep, tortoises, and turtles), illustrating various behaviors, including foraging, walking, and environmental scanning. We also propose correcting head orientations for body orientations to highlight specific heading-independent head rotation, and propose the derivation of O-sphere-metrics, such as angular speed across the sphere. This should help identify the functions of various head behaviors.Visualizations of the O-sphere provide an intuitive representation of animal behavior manifest via head orientation and rotation. This has ramifications for quantifying and understanding behaviors ranging from navigation through vigilance to feeding and, when used in tandem with body movement, should provide an important link between perception of the environment and response to it in free-ranging animals.

Optimizing the use of biologgers for movement ecology research.

The paradigm-changing opportunities of biologging sensors for ecological research, especially movement ecology, are vast, but the crucial questions of how best to match the most appropriate sensors and sensor combinations to specific biological questions and how to analyse complex biologging data, are mostly ignored. Here, we fill this gap by reviewing how to optimize the use of biologging techniques to answer questions in movement ecology and synthesize this into an Integrated Biologging Framework (IBF). We highlight that multisensor approaches are a new frontier in biologging, while identifying current limitations and avenues for future development in sensor technology. We focus on the importance of efficient data exploration, and more advanced multidimensional visualization methods, combined with appropriate archiving and sharing approaches, to tackle the big data issues presented by biologging. We also discuss the challenges and opportunities in matching the peculiarities of specific sensor data to the statistical models used, highlighting at the same time the large advances which will be required in the latter to properly analyse biologging data. Taking advantage of the biologging revolution will require a large improvement in the theoretical and mathematical foundations of movement ecology, to include the rich set of high-frequency multivariate data, which greatly expand the fundamentally limited and coarse data that could be collected using location-only technology such as GPS. Equally important will be the establishment of multidisciplinary collaborations to catalyse the opportunities offered by current and future biologging technology. If this is achieved, clear potential exists for developing a vastly improved mechanistic understanding of animal movements and their roles in ecological processes and for building realistic predictive models.

Social eavesdropping allows for a more risky gliding strategy by thermal-soaring birds.

Vultures are thought to form networks in the sky, with individuals monitoring the movements of others to gain up-to-date information on resource availability. While it is recognized that social information facilitates the search for carrion, how this facilitates the search for updrafts, another critical resource, remains unknown. In theory, birds could use information on updraft availability to modulate their flight speed, increasing their airspeed when informed on updraft location. In addition, the stylized circling behaviour associated with thermal soaring is likely to provide social cues on updraft availability for any bird operating in the surrounding area. We equipped five Gyps vultures with GPS and airspeed loggers to quantify the movements of birds flying in the same airspace. Birds that were socially informed on updraft availability immediately adopted higher airspeeds on entering the inter-thermal glide; a strategy that would be risky if birds were relying on personal information alone. This was embedded within a broader pattern of a reduction in airspeed (approx. 3 m s-1) through the glide, likely reflecting the need for low speed to sense and turn into the next thermal. Overall, this demonstrates (i) the complexity of factors affecting speed selection over fine temporal scales and (ii) that Gyps vultures respond to social information on the occurrence of energy in the aerial environment, which may reduce uncertainty in their movement decisions.

Vultures respond to challenges of near-ground thermal soaring by varying bank angle.

Many large birds rely on thermal soaring flight to travel cross-country. As such, they are under selective pressure to minimise the time spent gaining altitude in thermal updrafts. Birds should be able to maximise their climb rates by maintaining a position close to the thermal core through careful selection of bank angle and airspeed; however, there have been few direct measurements of either parameter. Here, we apply a novel methodology to quantify the bank angles selected by soaring birds using on-board magnetometers. We couple these data with airspeed measurements to parameterise the soaring envelope of two species of Gyps vulture, from which it is possible to predict 'optimal' bank angles. Our results show that these large birds respond to the challenges of gaining altitude in the initial phase of the climb, where thermal updrafts are weak and narrow, by adopting relatively high, and conserved, bank angles (25-35 deg). The bank angle decreased with increasing altitude, in a manner that was broadly consistent with a strategy of maximising the rate of climb. However, the lift coefficients estimated in our study were lower than those predicted by theoretical models and wind-tunnel studies. Overall, our results highlight how the relevant currency for soaring performance changes within individual climbs: when thermal radius is limiting, birds vary bank angle and maintain a constant airspeed, but speed increases later in the climb in order to respond to decreasing air density.

Identification of animal movement patterns using tri-axial magnetometry.

BACKGROUND: Accelerometers are powerful sensors in many bio-logging devices, and are increasingly allowing researchers to investigate the performance, behaviour, energy expenditure and even state, of free-living animals. Another sensor commonly used in animal-attached loggers is the magnetometer, which has been primarily used in dead-reckoning or inertial measurement tags, but little outside that. We examine the potential of magnetometers for helping elucidate the behaviour of animals in a manner analogous to, but very different from, accelerometers. The particular responses of magnetometers to movement means that there are instances when they can resolve behaviours that are not easily perceived using accelerometers. METHODS: We calibrated the tri-axial magnetometer to rotations in each axis of movement and constructed 3-dimensional plots to inspect these stylised movements. Using the tri-axial data of Daily Diary tags, attached to individuals of number of animal species as they perform different behaviours, we used these 3-d plots to develop a framework with which tri-axial magnetometry data can be examined and introduce metrics that should help quantify movement and behaviour.. RESULTS: Tri-axial magnetometry data reveal patterns in movement at various scales of rotation that are not always evident in acceleration data. Some of these patterns may be obscure until visualised in 3D space as tri-axial spherical plots (m-spheres). A tag-fitted animal that rotates in heading while adopting a constant body attitude produces a ring of data around the pole of the m-sphere that we define as its Normal Operational Plane (NOP). Data that do not lie on this ring are created by postural rotations of the animal as it pitches and/or rolls. Consequently, stereotyped behaviours appear as specific trajectories on the sphere (m-prints), reflecting conserved sequences of postural changes (and/or angular velocities), which result from the precise relationship between body attitude and heading. This novel approach shows promise for helping researchers to identify and quantify behaviours in terms of animal body posture, including heading. CONCLUSION: Magnetometer-based techniques and metrics can enhance our capacity to identify and examine animal behaviour, either as a technique used alone, or one that is complementary to tri-axial accelerometry.

In search of rules behind environmental framing; the case of head pitch.

BACKGROUND: Whether, and how, animals move requires them to assess their environment to determine the most appropriate action and trajectory, although the precise way the environment is scanned has been little studied. We hypothesized that head attitude, which effectively frames the environment for the eyes, and the way it changes over time, would be modulated by the environment. METHOD: To test this, we used a head-mounted device (Human-Interfaced Personal Observation platform - HIPOP) on people moving through three different environments; a botanical garden ('green' space), a reef ('blue' space), and a featureless corridor, to examine if head movement in the vertical axis differed between environments. Template matching was used to identify and quantify distinct behaviours. CONCLUSIONS: The data on head pitch from all subjects and environments over time showed essentially continuous clear waveforms with varying amplitude and wavelength. There were three stylised behaviours consisting of smooth, regular peaks and troughs in head pitch angle and variable length fixations during which the head pitch remained constant. These three behaviours accounted for ca. 40 % of the total time, with irregular head pitch changes accounting for the rest. There were differences in rates of manifestation of behaviour according to environment as well as environmentally different head pitch values of peaks, troughs and fixations. Finally, although there was considerable variation in head pitch angles, the peak and trough values bounded most of the variation in the fixation pitch values. It is suggested that the constant waveforms in head pitch serve to inform people about their environment, providing a scanning mechanism. Particular emphasis to certain sectors is manifest within the peak and trough limits and these appear modulated by the distribution of the points where fixation, interpreted as being due to objects of interest, occurs. This behaviour explains how animals allocate processing resources to the environment and shows promise for movement studies attempting to elucidate which parts of the environment affect movement trajectories.

Prying into the intimate secrets of animal lives; software beyond hardware for comprehensive annotation in 'Daily Diary' tags.

BACKGROUND: Smart tags attached to freely-roaming animals recording multiple parameters at infra-second rates are becoming commonplace, and are transforming our understanding of the way wild animals behave. Interpretation of such data is complex and currently limits the ability of biologists to realise the value of their recorded information. DESCRIPTION: This work presents Framework4, an all-encompassing software suite which operates on smart sensor data to determine the 4 key elements considered pivotal for movement analysis from such tags (Endangered Species Res 4: 123-37, 2008). These are; animal trajectory, behaviour, energy expenditure and quantification of the environment in which the animal moves. The program transforms smart sensor data into dead-reckoned movements, template-matched behaviours, dynamic body acceleration-derived energetics and position-linked environmental data before outputting it all into a single file. Biologists are thus left with a single data set where animal actions and environmental conditions can be linked across time and space. CONCLUSIONS: Framework4 is a user-friendly software that assists biologists in elucidating 4 key aspects of wild animal ecology using data derived from tags with multiple sensors recording at high rates. Its use should enhance the ability of biologists to derive meaningful data rapidly from complex data.

A multinational outbreak of histoplasmosis following a biology field trip in the Ugandan rainforest.

BACKGROUND: Outbreaks of histoplasmosis have been increasingly reported in association with travel to endemic areas. Multiple outbreaks have been reported following travel to the Americas, but reports of pulmonary histoplasmosis in short-term immunocompetent travelers to Africa are rare. METHODS: A biology student was referred to our unit with suspected pulmonary histoplasmosis following her return from a field trip in the Ugandan rainforest. The patient informed us that several of her multinational student colleagues on the same expedition had developed a similar illness. Using an alert in ProMED-mail and a questionnaire forwarded to each of the symptomatic students, we accumulated data on the other cases involved in this apparent outbreak of pulmonary histoplasmosis. RESULTS: Thirteen of 24 students developed respiratory symptoms following the expedition. Chest X-ray appearances were often suggestive of miliary tuberculosis but in most cases a final diagnosis of histoplasmosis was made (confirmed with serology in five cases, clinically diagnosed in six, and retrospectively suspected in two). Detailed questioning indicated that the likely source was a large hollow bat-infested tree within the rainforest. CONCLUSIONS: This is an unusual outbreak of histoplasmosis following short-term travel to Africa. Pulmonary histoplasmosis should always be considered in the differential diagnosis of an acute febrile respiratory illness in travelers returning from endemic areas or reporting activities suggesting exposure.