Examination of head versus body heading may help clarify the extent to which animal movement pathways are structured by environmental cues?

Understanding the processes that determine how animals allocate time to space is a major challenge, although it is acknowledged that summed animal movement pathways over time must define space-time use. The critical question is then, what processes structure these pathways? Following the idea that turns within pathways might be based on environmentally determined decisions, we equipped Arabian oryx with head- and body-mounted tags to determine how they orientated their heads - which we posit is indicative of them assessing the environment - in relation to their movement paths, to investigate the role of environment scanning in path tortuosity. After simulating predators to verify that oryx look directly at objects of interest, we recorded that, during routine movement, > 60% of all turns in the animals' paths, before being executed, were preceded by a change in head heading that was not immediately mirrored by the body heading: The path turn angle (as indicated by the body heading) correlated with a prior change in head heading (with head heading being mirrored by subsequent turns in the path) twenty-one times more than when path turns occurred due to the animals adopting a body heading that went in the opposite direction to the change in head heading. Although we could not determine what the objects of interest were, and therefore the proposed reasons for turning, we suggest that this reflects the use of cephalic senses to detect advantageous environmental features (e.g. food) or to detect detrimental features (e.g. predators). The results of our pilot study suggest how turns might emerge in animal pathways and we propose that examination of points of inflection in highly resolved animal paths could represent decisions in landscapes and their examination could enhance our understanding of how animal pathways are structured.

Wearable sensors for monitoring marine environments and their inhabitants.

Human societies depend on marine ecosystems, but their degradation continues. Toward mitigating this decline, new and more effective ways to precisely measure the status and condition of marine environments are needed alongside existing rebuilding strategies. Here, we provide an overview of how sensors and wearable technology developed for humans could be adapted to improve marine monitoring. We describe barriers that have slowed the transition of this technology from land to sea, update on the developments in sensors to advance ocean observation and advocate for more widespread use of wearables on marine organisms in the wild and in aquaculture. We propose that large-scale use of wearables could facilitate the concept of an 'internet of marine life' that might contribute to a more robust and effective observation system for the oceans and commercial aquaculture operations. These observations may aid in rationalizing strategies toward conservation and restoration of marine communities and habitats.

Impact of test, vaccinate or remove protocol on home ranges and nightly movements of badgers a medium density population.

In the British Isles, the European badger (Meles meles) is thought to be the primary wildlife reservoir of bovine tuberculosis (bTB), an endemic disease in cattle. Test, vaccinate or remove ('TVR') of bTB test-positive badgers, has been suggested to be a potentially useful protocol to reduce bTB incidence in cattle. However, the practice of removing or culling badgers is controversial both for ethical reasons and because there is no consistent observed effect on bTB levels in cattle. While removing badgers reduces population density, it may also result in disruption of their social behaviour, increase their ranging, and lead to greater intra- and inter-species bTB transmission. This effect has been recorded in high badger density areas, such as in southwest England. However, little is known about how TVR affects the behaviour and movement of badgers within a medium density population, such as those that occur in Northern Ireland (NI), which the current study aimed to examine. During 2014-2017, badger ranging behaviours were examined prior to and during a TVR protocol in NI. Nightly distances travelled by 38 individuals were determined using Global Positioning System (GPS) measurements of animal tracks and GPS-enhanced dead-reckoned tracks. The latter was calculated using GPS, tri-axial accelerometer and tri-axial magnetometer data loggers attached to animals. Home range and core home range size were measured using 95% and 50% autocorrelated kernel density estimates, respectively, based on location fixes. TVR was not associated with measured increases in either distances travelled per night (mean = 3.31 ± 2.64 km) or home range size (95% mean = 1.56 ± 0.62 km2, 50% mean = 0.39 ± 0.62 km2) over the four years of study. However, following trapping, mean distances travelled per night increased by up to 44% eight days post capture. Findings differ from those observed in higher density badger populations in England, in which badger ranging increased following culling. Whilst we did not assess behaviours of individual badgers, possible reasons why no differences in home range size were observed include higher inherent 'social fluidity' in Irish populations whereby movements are less restricted by habitat saturation and/or that the numbers removed did not reach a threshold that might induce increases in ranging behaviour. Nevertheless, short-term behavioural disruption from trapping was observed, which led to significant increases in the movements of individual animals within their home range. Whether or not TVR may alter badger behaviours remains to be seen, but it would be better to utilise solutions such as oral vaccination of badgers and/or cattle as well as increased biosecurity to limit bTB transmission, which may be less likely to cause interference and thereby reduce the likelihood of bTB transmission.

Highlighting when animals expend excessive energy for travel using dynamic body acceleration.

Travel represents a major cost for many animals so there should be selection pressure for it to be efficient - at minimum cost. However, animals sometimes exceed minimum travel costs for reasons that must be correspondingly important. We use Dynamic Body Acceleration (DBA), an acceleration-based metric, as a proxy for movement-based power, in tandem with vertical velocity (rate of change in depth) in a shark (Rhincodon typus) to derive the minimum estimated power required to swim at defined vertical velocities. We show how subtraction of measured DBA from the estimated minimum power for any given vertical velocity provides a "proxy for power above minimum" metric (PPAmin), highlighting when these animals travel above minimum power. We suggest that the adoption of this metric across species has value in identifying where and when animals are subject to compelling conditions that lead them to deviate from ostensibly judicious energy expenditure.

Wake respirometry allows breath-by-breath assessment of ventilation and CO2 production in unrestrained animals.

Quantifying stress and energetic responses in animals are major challenges, as existing methods lack temporal resolution and elevate animal stress. We propose "wake respirometry," a new method of quantifying fine-scale changes in CO2 production in unrestrained animals, using a nondispersive infrared CO2 sensor positioned downwind of the animal, i.e., in its wake. We parameterize the dispersion of CO2 in wakes using known CO2 flow rates and wind speeds. Tests with three bird species in a wind tunnel demonstrated that the system can resolve breath-by-breath changes in CO2 concentration, with clear exhalation signatures increasing in period and integral with body size. Changes in physiological state were detectable following handling, flight, and exposure to a perceived threat. We discuss the potential of wake respirometry to quantify stress and respiratory patterns in wild animals and provide suggestions for estimating behavior-specific metabolic rates via full integration of CO2 production across the wake.

Ecological inference using data from accelerometers needs careful protocols.

Accelerometers in animal-attached tags are powerful tools in behavioural ecology, they can be used to determine behaviour and provide proxies for movement-based energy expenditure. Researchers are collecting and archiving data across systems, seasons and device types. However, using data repositories to draw ecological inference requires a good understanding of the error introduced according to sensor type and position on the study animal and protocols for error assessment and minimisation.Using laboratory trials, we examine the absolute accuracy of tri-axial accelerometers and determine how inaccuracies impact measurements of dynamic body acceleration (DBA), a proxy for energy expenditure, in human participants. We then examine how tag type and placement affect the acceleration signal in birds, using pigeons Columba livia flying in a wind tunnel, with tags mounted simultaneously in two positions, and back- and tail-mounted tags deployed on wild kittiwakes Rissa tridactyla. Finally, we present a case study where two generations of tag were deployed using different attachment procedures on red-tailed tropicbirds Phaethon rubricauda foraging in different seasons.Bench tests showed that individual acceleration axes required a two-level correction to eliminate measurement error. This resulted in DBA differences of up to 5% between calibrated and uncalibrated tags for humans walking at a range of speeds. Device position was associated with greater variation in DBA, with upper and lower back-mounted tags varying by 9% in pigeons, and tail- and back-mounted tags varying by 13% in kittiwakes. The tropicbird study highlighted the difficulties of attributing changes in signal amplitude to a single factor when confounding influences tend to covary, as DBA varied by 25% between seasons.Accelerometer accuracy, tag placement and attachment critically affect the signal amplitude and thereby the ability of the system to detect biologically meaningful phenomena. We propose a simple method to calibrate accelerometers that can be executed under field conditions. This should be used prior to deployments and archived with resulting data. We also suggest a way that researchers can assess accuracy in previously collected data, and caution that variable tag placement and attachment can increase sensor noise and even generate trends that have no biological meaning.

The extinct shark Otodus megalodon was a transoceanic superpredator: Inferences from 3D modeling.

Although shark teeth are abundant in the fossil record, their bodies are rarely preserved. Thus, our understanding of the anatomy of the extinct Otodus megalodon remains rudimentary. We used an exceptionally well-preserved fossil to create the first three-dimensional model of the body of this giant shark and used it to infer its movement and feeding ecology. We estimate that an adult O. megalodon could cruise at faster absolute speeds than any shark species today and fully consume prey the size of modern apex predators. A dietary preference for large prey potentially enabled O. megalodon to minimize competition and provided a constant source of energy to fuel prolonged migrations without further feeding. Together, our results suggest that O. megalodon played an important ecological role as a transoceanic superpredator. Hence, its extinction likely had large impacts on global nutrient transfer and trophic food webs.

Long walk home: Magellanic penguins have strategies that lead them to areas where they can navigate most efficiently.

Understanding how animals move in dense environments where vision is compromised is a major challenge. We used GPS and dead-reckoning to examine the movement of Magellanic penguins commuting through vegetation that precluded long-distance vision. Birds leaving the nest followed the shortest, quickest route to the sea (the 'ideal path', or 'I-path') but return tracks depended where the birds left the water. Penguins arriving at the beach departure spot mirrored the departure. Most of those landing at a distance from the departure spot travelled slowly, obliquely to the coast at a more acute angle than a beeline trajectory to the nest. On crossing their I-path, these birds then followed this route quickly to their nests. This movement strategy saves birds distance, time and energy compared to a route along the beach and the into the colony on the I-track and saves time and energy compared to a beeline trajectory which necessitates slow travel in unfamiliar areas. This suggests that some animals adopt tactics that take them to an area where their navigational capacities are enhanced for efficient travel in challenging environments.

Decision rules for determining terrestrial movement and the consequences for filtering high-resolution global positioning system tracks: a case study using the African lion (Panthera leo).

The combined use of global positioning system (GPS) technology and motion sensors within the discipline of movement ecology has increased over recent years. This is particularly the case for instrumented wildlife, with many studies now opting to record parameters at high (infra-second) sampling frequencies. However, the detail with which GPS loggers can elucidate fine-scale movement depends on the precision and accuracy of fixes, with accuracy being affected by signal reception. We hypothesized that animal behaviour was the main factor affecting fix inaccuracy, with inherent GPS positional noise (jitter) being most apparent during GPS fixes for non-moving locations, thereby producing disproportionate error during rest periods. A movement-verified filtering (MVF) protocol was constructed to compare GPS-derived speed data with dynamic body acceleration, to provide a computationally quick method for identifying genuine travelling movement. This method was tested on 11 free-ranging lions (Panthera leo) fitted with collar-mounted GPS units and tri-axial motion sensors recording at 1 and 40 Hz, respectively. The findings support the hypothesis and show that distance moved estimates were, on average, overestimated by greater than 80% prior to GPS screening. We present the conceptual and mathematical protocols for screening fix inaccuracy within high-resolution GPS datasets and demonstrate the importance that MVF has for avoiding inaccurate and biased estimates of movement.

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.

Animal lifestyle affects acceptable mass limits for attached tags.

Animal-attached devices have transformed our understanding of vertebrate ecology. To minimize any associated harm, researchers have long advocated that tag masses should not exceed 3% of carrier body mass. However, this ignores tag forces resulting from animal movement. Using data from collar-attached accelerometers on 10 diverse free-ranging terrestrial species from koalas to cheetahs, we detail a tag-based acceleration method to clarify acceptable tag mass limits. We quantify animal athleticism in terms of fractions of animal movement time devoted to different collar-recorded accelerations and convert those accelerations to forces (acceleration × tag mass) to allow derivation of any defined force limits for specified fractions of any animal's active time. Specifying that tags should exert forces that are less than 3% of the gravitational force exerted on the animal's body for 95% of the time led to corrected tag masses that should constitute between 1.6% and 2.98% of carrier mass, depending on athleticism. Strikingly, in four carnivore species encompassing two orders of magnitude in mass (ca 2-200 kg), forces exerted by '3%' tags were equivalent to 4-19% of carrier body mass during moving, with a maximum of 54% in a hunting cheetah. This fundamentally changes how acceptable tag mass limits should be determined by ethics bodies, irrespective of the force and time limits specified.

Animal tag technology keeps coming of age: an engineering perspective.

Animal-borne tags (biologgers) have now become extremely sophisticated, recording data from multiple sensors at high frequencies for long periods and, as such, have become a powerful tool for behavioural ecologists and physiologists studying wild animals. But the design and implementation of these tags is not trivial because engineers have to maximize performance and ability to function under onerous conditions while minimizing tag mass and volume (footprint) to maximize the wellbeing of the animal carriers. We present some of the major issues faced by tag engineers and show how tag designers must accept compromises while maintaining systems that can answer the questions being posed. We also argue that basic understanding of engineering issues in tag design by biologists will help feedback to engineers to better tag construction but also reduce the likelihood that tag-deploying biologists will misunderstand their own results. Finally, we suggest that proper consideration of conventional technology together with new approaches will lead to further step changes in our understanding of wild-animal biology using smart tags. This article is part of the theme issue 'Measuring physiology in free-living animals (Part II)'.

Fine-scale changes in speed and altitude suggest protean movements in homing pigeon flights.

The power curve provides a basis for predicting adjustments that animals make in flight speed, for example in relation to wind, distance, habitat foraging quality and objective. However, relatively few studies have examined how animals respond to the landscape below them, which could affect speed and power allocation through modifications in climb rate and perceived predation risk. We equipped homing pigeons (Columba livia) with high-frequency loggers to examine how flight speed, and hence effort, varies in relation to topography and land cover. Pigeons showed mixed evidence for an energy-saving strategy, as they minimized climb rates by starting their ascent ahead of hills, but selected rapid speeds in their ascents. Birds did not modify their speed substantially in relation to land cover, but used higher speeds during descending flight, highlighting the importance of considering the rate of change in altitude before estimating power use from speed. Finally, we document an unexpected variability in speed and altitude over fine scales; a source of substantial energetic inefficiency. We suggest this may be a form of protean behaviour adopted to reduce predation risk when flocking is not an option, and that such a strategy could be widespread.

Accidents alter animal fitness landscapes.

Animals alter their habitat use in response to the energetic demands of movement ('energy landscapes') and the risk of predation ('the landscape of fear'). Recent research suggests that animals also select habitats and move in ways that minimise their chance of temporarily losing control of movement and thereby suffering slips, falls, collisions or other accidents, particularly when the consequences are likely to be severe (resulting in injury or death). We propose that animals respond to the costs of an 'accident landscape' in conjunction with predation risk and energetic costs when deciding when, where, and how to move in their daily lives. We develop a novel theoretical framework describing how features of physical landscapes interact with animal size, morphology, and behaviour to affect the risk and severity of accidents, and predict how accident risk might interact with predation risk and energetic costs to dictate movement decisions across the physical landscape. Future research should focus on testing the hypotheses presented here for different real-world systems to gain insight into the relative importance of theorised effects in the field.

Genetic divergence and evidence of human-mediated translocation of two-fingered sloths (Choloepus hoffmanni) in Costa Rica.

Sloths are notoriously slow and consequently have limited dispersal ability, which makes them particularly vulnerable to the effects of habitat fragmentation and degradation. Sloths in Costa Rica are considered of conservation concern due to habitat loss, livestock production and increasing urbanization. Reintroductions from rescue centres are commonplace across the country, yet their genetic diversity and population structure are unknown, and there is currently little consideration of the genetic background prior to intervention or releases. We used microsatellite analysis to undertake the first exploratory investigation into sloth population genetics in Costa Rica. Using data from 98 two-fingered sloths (Choloepus hoffmanni) from four different geographic regions, we determined the presence of four potential genetic groups, three of them with minimal population structuring despite the limited dispersal ability and presence of physical barriers. Sloths from the North appear to represent a highly distinct population that we propose may require management as a discrete unit for conservation. We stress the need for additional analyses to better understand the genetic structure and diversity of North andWest regions and suggest that rescue facilities in Costa Rica should consider the genetic background of rehabilitated sloths when planning future reintroductions. Our results also highlight the threat posed by physical isolation due to widespread urbanization and agriculture expansion for a species with a weak dispersal ability.

A new direction for differentiating animal activity based on measuring angular velocity about the yaw axis.

The use of animal-attached data loggers to quantify animal movement has increased in popularity and application in recent years. High-resolution tri-axial acceleration and magnetometry measurements have been fundamental in elucidating fine-scale animal movements, providing information on posture, traveling speed, energy expenditure, and associated behavioral patterns. Heading is a key variable obtained from the tandem use of magnetometers and accelerometers, although few field investigations have explored fine-scale changes in heading to elucidate differences in animal activity (beyond the notable exceptions of dead-reckoning).This paper provides an overview of the value and use of animal heading and a prime derivative, angular velocity about the yaw axis, as an important element for assessing activity extent with potential to allude to behaviors, using "free-ranging" Loggerhead turtles (Caretta caretta) as a model species.We also demonstrate the value of yaw rotation for assessing activity extent, which varies over the time scales considered and show that various scales of body rotation, particularly rate of change of yaw, can help resolve differences between fine-scale behavior-specific movements. For example, oscillating yaw movements about a central point of the body's arc implies bouts of foraging, while unusual circling behavior, indicative of conspecific interactions, could be identified from complete revolutions of the longitudinal axis.We believe this approach should help identification of behaviors and "space-state" approaches to enhance our interpretation of behavior-based movements, particularly in scenarios where acceleration metrics have limited value, such as for slow-moving animals.

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.

Estimates for energy expenditure in free-living animals using acceleration proxies: A reappraisal.

It is fundamentally important for many animal ecologists to quantify the costs of animal activities, although it is not straightforward to do so. The recording of triaxial acceleration by animal-attached devices has been proposed as a way forward for this, with the specific suggestion that dynamic body acceleration (DBA) be used as a proxy for movement-based power. Dynamic body acceleration has now been validated frequently, both in the laboratory and in the field, although the literature still shows that some aspects of DBA theory and practice are misunderstood. Here, we examine the theory behind DBA and employ modelling approaches to assess factors that affect the link between DBA and energy expenditure, from the deployment of the tag, through to the calibration of DBA with energy use in laboratory and field settings. Using data from a range of species and movement modes, we illustrate that vectorial and additive DBA metrics are proportional to each other. Either can be used as a proxy for energy and summed to estimate total energy expended over a given period, or divided by time to give a proxy for movement-related metabolic power. Nonetheless, we highlight how the ability of DBA to predict metabolic rate declines as the contribution of non-movement-related factors, such as heat production, increases. Overall, DBA seems to be a substantive proxy for movement-based power but consideration of other movement-related metrics, such as the static body acceleration and the rate of change of body pitch and roll, may enable researchers to refine movement-based metabolic costs, particularly in animals where movement is not characterized by marked changes in body acceleration.