Meteorological and environmental variables affect flight behaviour and decision‐making of an obligate soaring bird,the California Condor Gymnogyps californianus

The movements of animals are limited by evolutionary constraints and ecological processes and are strongly influenced by the medium through which they travel. For flying animals, variation in atmospheric conditions is critically influential in movement. Obligate soaring birds depend on external sources of updraft more than do other flying species, as without that updraft they are unable to sustain flight for extended periods. These species are therefore good models for understanding how the environment can influence decisions about movement. We used meteorological and topographic variables to understand the environmental influences on the decision to engage in flight by obligate soaring and critically endangered California Condors Gymnogyps californianus. Condors were more likely to fly, soared at higher altitudes and flew over smoother terrain when weather conditions promoted either thermal or orographic updrafts, for example when turbulence and solar radiation were higher and when winds from the east and north were stronger. However, increased atmospheric stability, which is inconsistent with thermal development but may be associated with orographic updrafts, was correlated with a somewhat higher probability of being in flight at lower altitudes and over rougher terrain. The close and previously undescribed linkages between Condor flight and conditions that support development of thermal and orographic updrafts provide important insight into the behaviour of obligate soaring birds and into the environmental parameters that may define the currently expanding distribution of Condors within and outside the state of California.     

Flight responses by a migratory soaring raptor to changing meteorological conditions

Soaring birds that undertake long-distance migration should develop strategies to minimize the energetic costs of endurance flight. This is relevant because condition upon completion of migration has direct consequences for fecundity, fitness and thus, demography. Therefore, strong evolutionary pressures are expected for energy minimization tactics linked to weather and topography. Importantly, the minute-by-minute mechanisms birds use to subsidize migration in variable weather are largely unknown, in large part because of the technological limitations in studying detailed long-distance bird flight. Here, we show golden eagle (Aquila chrysaetos) migratory response to changing meteorological conditions as monitored by high-resolution telemetry. In contrast to expectations, responses to meteorological variability were stereotyped across the 10 individuals studied. Eagles reacted to increased wind speed by using more orographic lift and less thermal lift. Concomitantly, as use of thermals decreased, variation in flight speed and altitude also decreased. These results demonstrate how soaring migrant birds can minimize energetic expenditures, they show the context for avian decisions and choices of specific instantaneous flight mechanisms and they have important implications for design of bird-friendly wind energy.     

Nutritional state and collective motion: from individuals to mass migration

In order to move effectively in unpredictable or heterogeneous environments animals must make appropriate decisions in response to internal and external cues. Identifying the link between these components remains a challenge for movement ecology and is important in understanding the mechanisms driving both individual and collective motion. One accessible way of examining how internal state influences an individual''s motion is to consider the nutritional state of an animal. Our experimental results reveal that nutritional state exerts a relatively minor influence on the motion of isolated individuals, but large group-level differences emerge from diet affecting inter-individual interactions. This supports the idea that mass movement in locusts may be driven by cannibalism. To estimate how these findings are likely to impact collective migration of locust hopper bands, we create an experimentally parametrized model of locust interactions and motion. Our model supports our hypothesis that nutrient-dependent social interactions can lead to the collective motion seen in our experiments and predicts a transition in the mean speed and the degree of coordination of bands with increasing insect density. Furthermore, increasing the interaction strength (representing greater protein deprivation) dramatically reduces the critical density at which this transition occurs, demonstrating that individuals'' nutritional state could have a major impact on large-scale migration.     

Gravity-defying Behaviors: Identifying Models for Protoaves

Most current phylogenetic hypotheses based upon cladistic methodologyassert that birds are the direct descendants of derived maniraptorantheropod dinosaurs, and that the origin of avian flight necessarilydeveloped within a terrestrial context (i.e., from the "groundup"). Most theoretical aerodynamic and energetic models or chronologicallyappropriate fossil data do not support these hypotheses forthe evolution of powered flight. The more traditional modelfor the origin of flight derives birds from among small arborealearly Mesozoic archosaurs ("thecodonts"). According to thismodel, protoavian ancestors developed flight in the trees viaa series of intermediate stages, such as leaping, parachuting,gliding, and flapping. This model benefits from the assemblageof living and extinct arboreal vertebrates that engage in analogousnon-powered aerial activities using elevation as a source ofgravitational energy. Recent reports of "feathered theropods"notwithstanding, the evolution of birds from any known groupof maniraptoran theropods remains equivocal.     

The evolution of predictive adaptive responses in human life history

Many studies in humans have shown that adverse experience in early life is associated with accelerated reproductive timing, and there is comparative evidence for similar effects in other animals. There are two different classes of adaptive explanation for associations between early-life adversity and accelerated reproduction, both based on the idea of predictive adaptive responses (PARs). According to external PAR hypotheses, early-life adversity provides a ‘weather forecast’ of the environmental conditions into which the individual will mature, and it is adaptive for the individual to develop an appropriate phenotype for this anticipated environment. In internal PAR hypotheses, early-life adversity has a lasting negative impact on the individual''s somatic state, such that her health is likely to fail more rapidly as she gets older, and there is an advantage to adjusting her reproductive schedule accordingly. We use a model of fluctuating environments to derive evolveability conditions for acceleration of reproductive timing in response to early-life adversity in a long-lived organism. For acceleration to evolve via the external PAR process, early-life cues must have a high degree of validity and the level of annual autocorrelation in the individual''s environment must be almost perfect. For acceleration to evolve via the internal PAR process requires that early-life experience must determine a significant fraction of the variance in survival prospects in adulthood. The two processes are not mutually exclusive, and mechanisms for calibrating reproductive timing on the basis of early experience could evolve through a combination of the predictive value of early-life adversity for the later environment and its negative impact on somatic state.     

Body mass variation in breeding Florida Scrub‐Jays

ABSTRACT Many birds lose mass when feeding dependent young and multiple hypotheses have been proposed to explain this loss. The reproductive‐stress hypothesis suggests that mass loss results from an energy deficit. The flight‐efficiency hypothesis suggests that breeders lose mass in advance of feeding young to save energy during flight. The reserve‐mobilization hypothesis suggests that female breeders accumulate energy reserves during egg production and incubation and mobilize those reserves to meet their own energy needs after eggs hatch. Finally, birds may lose mass due to gonadal regression. From 1999 to 2001, we attracted Florida Scrub‐Jays (Aphelocoma coerulescens), sedentary cooperative breeders, to a portable electronic balance. Our objective was to determine which hypotheses might best explain mass variation during breeding. Both male and female Florida Scrub‐Jays lost mass during the period of nestling care (males, 3.2%; females, 6.5%), but not when feeding fledglings, despite this being the period of peak effort. Such results are consistent with both the flight‐efficiency and reserve‐mobilization (females only) hypotheses. We also found a significant negative influence of brood size on mass change in males, providing support for the reproductive‐stress hypothesis, and we conclude that, for males, both the flight‐efficiency and reproductive‐stress hypotheses apply. For female scrub‐jays, our results were consistent with the flight‐efficiency and energy‐reserve mobilization hypotheses, both of which view mass loss as beneficial.     

Flight mode affects allometry of migration range in birds

Billions of birds migrate to exploit seasonally available resources. The ranges of migration vary greatly among species, but the underlying mechanisms are poorly understood. I hypothesise that flight mode (flapping or soaring) and body mass affect migration range through their influence on flight energetics. Here, I compiled the tracks of migratory birds (196 species, weighing 12–10 350 g) recorded by electronic tags in the last few decades. In flapping birds, migration ranges decreased with body mass, as predicted from rapidly increasing flight cost with increasing body mass. The species with higher aspect ratio and lower wing loading had larger migration ranges. In soaring birds, migration ranges were mass‐independent and larger than those of flapping birds, reflecting their low flight costs irrespective of body mass. This study demonstrates that many animal‐tracking studies are now available to explore the general patterns and the underlying mechanisms of animal migration.     

Functional significance of emergence timing in bats

We investigated intraspecific differences in evening emergence time of northern bats Eptesicus nilssonii , greater horseshoe bats Rhinolophus ferrumequinum and lesser horseshoe bats R. hipposideros. Significant differences in emergence time were associated with presumed variation in predation risk, related to light intensity, and energetic benefits of early emergence, caused by differences in age, reproductive state (energetic demands), and body condition. Females of both species emerged progressively later as pregnancy advanced, perhaps because of decreased flight performance, and earlier as lactation proceeded, probably because of increased energy demands and low reserves. Bats under energetic stress, due to persistent low ambient temperatures during pregnancy, or when body reserves were low, emerged relatively early, and hence appeared to take higher risks, than other bats. Young bats emerged much later than the adults at first, but progressively earlier as their flight skills improved. Lesser horseshoe bats emerged later at exposed roost exits than in more protected situations. The results largely corroborate the hypothesis that emergence time, and therefore feeding performance, of insectivorous bats is constrained at bright light conditions, possibly by predation risk (from birds), and modified by energetic considerations.     

Energetic reserves of marsh tits (Parus palustris): food and fat storage in response to variable food supply

During the winter, small birds face the threat of starvationduring the day and overnight. The threat of starvation can bereduced by maintaining higher energetic reserves, either asinternal fat stores or as external hoards. I present here empiricaldata concerning the management of energetic reserves in responseto unpredictability in foraging success. Predictions of a modelwere tested using marsh tits (Parus palustris) experiencingconditions of low and high temporal variation in food supply.Under the high-variation treatment, birds increased externalhoards but not internal fat reserves. In addition, birds decreasedtheir mean hoard-recovery interval compared to conditions inwhich food was predictable. Detailed examination of body weightthroughout the day indicates that marsh tits delayed the accumulationof overnight fat reserves until relatively late in the day.Overall, these results support the theory that fat reservesare costly to acquire and maintain and suggest that marsh titsactively manage both internal and external energetic reserveswithin and among days.     

Flight performance in the altricial zebra finch: Developmental effects and reproductive consequences

The environmental conditions animals experience during development can have sustained effects on morphology, physiology, and behavior. Exposure to elevated levels of stress hormones (glucocorticoids, GCs) during development is one such condition that can have long‐term effects on animal phenotype. Many of the phenotypic effects of GC exposure during development (developmental stress) appear negative. However, there is increasing evidence that developmental stress can induce adaptive phenotypic changes. This hypothesis can be tested by examining the effect of developmental stress on fitness‐related traits. In birds, flight performance is an ideal metric to assess the fitness consequences of developmental stress. As fledglings, mastering takeoff is crucial to avoid bodily damage and escape predation. As adults, takeoff can contribute to mating and foraging success as well as escape and, thus, can affect both reproductive success and survival. We examined the effects of developmental stress on flight performance across life‐history stages in zebra finches (Taeniopygia guttata). Specifically, we examined the effects of oral administration of corticosterone (CORT, the dominant avian glucocorticoid) during development on ground‐reaction forces and velocity during takeoff. Additionally, we tested for associations between flight performance and reproductive success in adult male zebra finches. Developmental stress had no effect on flight performance at all ages. In contrast, brood size (an unmanipulated variable) had sustained, negative effects on takeoff performance across life‐history stages with birds from small broods performing better than birds from large broods. Flight performance at 100 days posthatching predicted future reproductive success in males; the best fliers had significantly higher reproductive success. Our results demonstrate that some environmental factors experienced during development (e.g. clutch size) have stronger, more sustained effects than others (e.g. GC exposure). Additionally, our data provide the first link between flight performance and a direct measure of reproductive success.     

Exploring the relationship between flapping behaviour and accelerometer signal during ascending flight,and a new approach to calibration

We understand little about the energetic costs of flight in free-ranging birds, in part because current techniques for estimating flight energetics in the wild are limited. Accelerometry is known to estimate energy expenditure through body movement in terrestrial animals, once calibrated using a treadmill with chamber respirometry. The flight equivalent, a wind tunnel with mask respirometry, is particularly difficult to instigate, and has not been applied to calibrate accelerometry. We take the first steps in exploring a novel method for calibrating accelerometers with flight energy expenditure. We collected accelerometry data for Harris's Hawks Parabuteo unicinctus flying to varying heights up to 4.1 m over a small horizontal distance; the mechanical energy expended to gain height can be estimated from physical first principles. The relationship between accelerometry and mechanical energy expenditure was strong, and while a simple wing flapping model confirmed that accelerometry is sensitive to both changes in wing beat amplitude and frequency, the relationship was explained predominately by changes in wing beat frequency, and less so by changes in amplitude. Our study provides initial, positive evidence that accelerometry can be calibrated with body power using climbing flights, potentially providing a basis for estimating flapping flight metabolic rate at least in situations of altitude gain.     

Migration by soaring or flapping: numerical atmospheric simulations reveal that turbulence kinetic energy dictates bee-eater flight mode

Aerial migrants commonly face atmospheric dynamics that may affect their movement and behaviour. Specifically, bird flight mode has been suggested to depend on convective updraught availability and tailwind assistance. However, this has not been tested thus far since both bird tracks and meteorological conditions are difficult to measure in detail throughout extended migratory flyways. Here, we applied, to our knowledge, the first comprehensive numerical atmospheric simulations by mean of the Regional Atmospheric Modeling System (RAMS) to study how meteorological processes affect the flight behaviour of migrating birds. We followed European bee-eaters (Merops apiaster) over southern Israel using radio telemetry and contrasted bird flight mode (flapping, soaring-gliding or mixed flight) against explanatory meteorological variables estimated by RAMS simulations at a spatial grid resolution of 250 × 250 m(2). We found that temperature and especially turbulence kinetic energy (TKE) determine bee-eater flight mode, whereas, unexpectedly, no effect of tailwind assistance was found. TKE during soaring-gliding was significantly higher and distinct from TKE during flapping. We propose that applying detailed atmospheric simulations over extended migratory flyways can elucidate the highly dynamic behaviour of air-borne organisms, help predict the abundance and distribution of migrating birds, and aid in mitigating hazardous implications of bird migration.     

Wind estimation based on thermal soaring of birds

The flight performance of birds is strongly affected by the dynamic state of the atmosphere at the birds' locations. Studies of flight and its impact on the movement ecology of birds must consider the wind to help us understand aerodynamics and bird flight strategies. Here, we introduce a systematic approach to evaluate wind speed and direction from the high‐frequency GPS recordings from bird‐borne tags during thermalling flight. Our method assumes that a fixed horizontal mean wind speed during a short (18 seconds, 19 GPS fixes) flight segment with a constant turn angle along a closed loop, characteristic of thermalling flight, will generate a fixed drift for each consequent location. We use a maximum‐likelihood approach to estimate that drift and to determine the wind and airspeeds at the birds' flight locations. We also provide error estimates for these GPS‐derived wind speed estimates. We validate our approach by comparing its wind estimates with the mid‐resolution weather reanalysis data from ECMWF, and by examining independent wind estimates from pairs of birds in a large dataset of GPS‐tagged migrating storks that were flying in close proximity. Our approach provides accurate and unbiased observations of wind speed and additional detailed information on vertical winds and uplift structure. These precise measurements are otherwise rare and hard to obtain and will broaden our understanding of atmospheric conditions, flight aerodynamics, and bird flight strategies. With an increasing number of GPS‐tracked animals, we may soon be able to use birds to inform us about the atmosphere they are flying through and thus improve future ecological and environmental studies.     

The role of wing length in the evolution of avian flightlessness

Flightlessness has evolved independently in at least 11 extant avian families. A number of hypotheses have been proposed to explain these transitions in individual families, including release from predation on oceanic islands, energetic costs of flight and use of forelimbs for activities other than flying. Few studies have sought to explore factors common to all families containing flightless species, which may explain the taxonomic distribution of flightlessness. In this study, we found that for all eight avian families which contain both flightless and flighted species, the flighted species have shorter wing lengths relative to body mass than their sister families. This result is not biased by taxon size. Models of avian aerodynamics predict that birds with relatively short wings pay a high energetic cost of flight. We suggest that these increased energetic costs of flying predispose these avian families to evolve flightless species. The various causes for the shortening of wings among flighted species of birds and the possibility of future transitions to flightlessness are discussed.     

State dependence,personality, and plants: light‐foraging decisions in Mimosa pudica (L.)

Plants make foraging decisions that are dependent on ecological conditions, such as resource availability and distribution. Despite the field of plant behavioral ecology gaining momentum, ecologists still know little about what factors impact plant behavior, especially light‐foraging behavior. We made use of the behavioral reaction norm approach to investigate light foraging in a plant species that exhibits rapid movement: Mimosa pudica. We explored how herbivore avoidance behavior in M. pudica (which closes its leaflets temporarily when disturbed) is affected by an individual's energy state and the quality of the current environment and also repeatedly tested the behavior of individuals from two seed sources to determine whether individuals exhibit a “personality” (i.e., behavioral syndrome). We found that when individuals are in a low‐energy state, they adopt a riskier light‐foraging strategy, opening leaflets faster, and not closing leaflets as often in response to a disturbance. However, when plants are in a high‐energy state, they exhibit a plastic light‐foraging strategy dependent on environment quality. Although we found no evidence that individuals exhibit behavioral syndromes, we found that individuals from different seed sources consistently behave differently from each other. Our results suggest that plants are capable of making state‐dependent decisions and that plant decision making is complex, depending on the interplay between internal and external factors.     

FORELIMB POSTURE IN DINOSAURS AND THE EVOLUTION OF THE AVIAN FLAPPING FLIGHT-STROKE

Ontogenetic and behavioral studies using birds currently do not document the early evolution of flight because birds (including juveniles) used in such studies employ forelimb oscillation frequencies over 10 Hz, forelimb stroke-angles in excess of 130°, and possess uniquely avian flight musculatures. Living birds are an advanced morphological stage in the development of flapping flight. To gain insight into the early stages of flight evolution (i.e., prebird), in the absence of a living analogue, a new approach using Strouhal number     was used. Strouhal number is a nondimensional number that describes the relationship between wing-stroke amplitude ( A ), wing-beat frequency ( f ), and flight speed ( U ). Calculations indicated that even moderate wing movements are enough to generate rudimentary thrust and that a propulsive flapping flight-stroke could have evolved via gradual incremental changes in wing movement and wing morphology. More fundamental to the origin of the avian flapping flight-stroke is the question of how a symmetrical forelimb posture—required for gliding and flapping flight—evolved from an alternating forelimb motion, evident in all extant bipeds when running except birds.     

sOAR: a tool for modelling optimal animal life‐history strategies in cyclic environments

Periodic environments determine the life cycle of many animals across the globe and the timing of important life history events, such as reproduction and migration. These adaptive behavioural strategies are complex and can only be fully understood (and predicted) within the framework of natural selection in which species adopt evolutionary stable strategies. We present sOAR, a powerful and user‐friendly implementation of the well‐established framework of optimal annual routine modelling. It allows determining optimal animal life history strategies under cyclic environmental conditions using stochastic dynamic programming. It further includes the simulation of population dynamics under the optimal strategy. sOAR provides an important tool for theoretical studies on the behavioural and evolutionary ecology of animals. It is especially suited for studying bird migration. In particular, we integrated options to differentiate between costs of active and passive flight into the optimal annual routine modelling framework, as well as options to consider periodic wind conditions affecting flight energetics. We provide an illustrative example of sOAR where food supply in the wintering habitat of migratory birds significantly alters the optimal timing of migration. sOAR helps improving our understanding of how complex behaviours evolve and how behavioural decisions are constrained by internal and external factors experienced by the animal. Such knowledge is crucial for anticipating potential species’ response to global environmental change.     

Temporal and Contextual Consistency of Leadership in Homing Pigeon Flocks

Organized flight of homing pigeons (Columba livia) was previously shown to rely on simple leadership rules between flock mates, yet the stability of this social structuring over time and across different contexts remains unclear. We quantified the repeatability of leadership-based flock structures within a flight and across multiple flights conducted with the same animals. We compared two contexts of flock composition: flocks of birds of the same age and flight experience; and, flocks of birds of different ages and flight experience. All flocks displayed consistent leadership-based structures over time, showing that individuals have stable roles in the navigational decisions of the flock. However, flocks of balanced age and flight experience exhibited reduced leadership stability, indicating that these factors promote flock structuring. Our study empirically demonstrates that leadership and followership are consistent behaviours in homing pigeon flocks, but such consistency is affected by the heterogeneity of individual flight experiences and/or age. Similar evidence from other species suggests leadership as an important mechanism for coordinated motion in small groups of animals with strong social bonds.     

Reproductive Energetics of Female Mantled Howlers (<Emphasis Type="Italic">Alouatta palliata</Emphasis>)

The energetic costs of reproduction have an important influence on the life histories of female primates. At present, however, the interplay of female reproductive state, food availability, and strategies aimed at maintaining energy balance has been described for only a few species, limiting our ability to understand intra- and interspecific variation in female life histories. We assessed how female mantled howlers (Alouatta palliata) are affected by reproductive seasonality, and whether they alter their behavior to cope with the energetic demands of reproduction. From August 2013 to July 2015 we measured the reproductive state, behavior (1100 h of focal animal observations), and energetic condition (312 urine samples collected for C-peptide analysis) of 7 adult females, and assessed food availability (weekly phenological sampling of 397 food trees). Female behavior did not vary with reproductive state or reproductive seasonality. There were, however, differences in how females responded to variation in food availability according to reproductive state. Cycling and gestating females spent more time feeding than lactating females, and cycling females less time resting than females in other reproductive states, when food was more available. C-peptide concentrations were unaffected by either individual or overall variation in reproductive state, except for cycling females, whose concentrations increased during periods of high food availability. The energetic condition of female mantled howlers is broadly maintained over different stages of reproduction, but is sensitive to variation in food availability.     

Object detection in the fly during simulated translatory flight

Translatory movement of an animal in its environment induces optic flow that contains information about the three-dimensional layout of the surroundings: as a rule, images of objects that are closer to the animal move faster across the retina than those of more distant objects. Such relative motion cues are used by flies to detect objects in front of a structured background. We confronted flying flies, tethered to a torque meter, with front-to-back motion of patterns displayed on two CRT screens, thereby simulating translatory motion of the background as experienced by an animal during straight flight. The torque meter measured the instantaneous turning responses of the fly around its vertical body axis. During short time intervals, object motion was superimposed on background pattern motion. The average turning response towards such an object depends on both object and background velocity in a characteristic way: (1) in order to elicit significant responses object motion has to be faster than background motion; (2) background motion within a certain range of velocities improves object detection. These properties can be interpreted as adaptations to situations as they occur in natural free flight. We confirmed that the measured responses were mediated mainly by a control system specialized for the detection of objects rather than by the compensatory optomotor system responsible for course stabilization. Accepted: 20 March 1997