The ways in which seabirds navigate over very large spatial scales remain poorly understood. While olfactory and visual information can provide guidance over short distances, their range is often limited to 100s km, far below the navigational capacity of wide-ranging animals such as albatrosses. Infrasound is a form of low-frequency sound that propagates for 1,000s km in the atmosphere. In marine habitats, its association with storms and ocean surface waves could in effect make it a useful cue for anticipating environmental conditions that favor or hinder flight or be associated with profitable foraging patches. However, behavioral responses of wild birds to infrasound remain untested. Here, we explored whether wandering albatrosses, Diomedea exulans, respond to microbarom infrasound at sea. We used Global Positioning System tracks of 89 free-ranging albatrosses in combination with acoustic modeling to investigate whether albatrosses preferentially orientate toward areas of 'loud' microbarom infrasound on their foraging trips. We found that in addition to responding to winds encountered in situ, albatrosses moved toward source regions associated with higher sound pressure levels. These findings suggest that albatrosses may be responding to long-range infrasonic cues. As albatrosses depend on winds and waves for soaring flight, infrasonic cues may help albatrosses to identify environmental conditions that allow them to energetically optimize flight over long distances. Our results shed light on one of the great unresolved mysteries in nature, navigation in seemingly featureless ocean environments.

Seabirds are amongst the most mobile of all animal species and spend large amounts of their lives at sea. They cross vast areas of ocean that appear superficially featureless, and our understanding of the mechanisms that they use for navigation remains incomplete, especially in terms of available cues. In particular, several large-scale navigational tasks, such as homing across thousands of kilometers to breeding sites, are not fully explained by visual, olfactory or magnetic stimuli. Low-frequency inaudible sound, i.e., infrasound, is ubiquitous in the marine environment. The spatio-temporal consistency of some components of the infrasonic wavefield, and the sensitivity of certain bird species to infrasonic stimuli, suggests that infrasound may provide additional cues for seabirds to navigate, but this remains untested. Here, we propose a framework to explore the importance of infrasound for navigation. We present key concepts regarding the physics of infrasound and review the physiological mechanisms through which infrasound may be detected and used. Next, we propose three hypotheses detailing how seabirds could use information provided by different infrasound sources for navigation as an acoustic beacon, landmark, or gradient. Finally, we reflect on strengths and limitations of our proposed hypotheses, and discuss several directions for future work. In particular, we suggest that hypotheses may be best tested by combining conceptual models of navigation with empirical data on seabird movements and in-situ infrasound measurements.

The perception of airborne infrasound (sounds below 20 Hz, inaudible to humans except at very high levels) has been documented in a handful of mammals and birds. While animals that produce vocalizations with infrasonic components (e.g. elephants) present conspicuous examples of potential use of infrasound in the context of communication, the extent to which airborne infrasound perception exists among terrestrial animals is unclear. Given that most infrasound in the environment arises from geophysical sources, many of which could be ecologically relevant, communication might not be the only use of infrasound by animals. Therefore, infrasound perception could be more common than currently realized. At least three bird species, each of which do not communicate using infrasound, are capable of detecting infrasound, but the associated auditory mechanisms are not well understood. Here we combine an evaluation of hearing measurements with anatomical observations to propose and evaluate hypotheses supporting avian infrasound detection. Environmental infrasound is mixed with non-acoustic pressure fluctuations that also occur at infrasonic frequencies. The ear can detect such non-acoustic pressure perturbations and therefore, distinguishing responses to infrasound from responses to non-acoustic perturbations presents a great challenge. Our review shows that infrasound could stimulate the ear through the middle ear (tympanic) route and by extratympanic routes bypassing the middle ear. While vibration velocities of the middle ear decline towards infrasonic frequencies, whole-body vibrations – which are normally much lower amplitude than that those of the middle ear in the ‘audible’ range (i.e. >20 Hz) – do not exhibit a similar decline and therefore may reach vibration magnitudes comparable to the middle ear at infrasonic frequencies. Low stiffness in the middle and inner ear is expected to aid infrasound transmission. In the middle ear, this could be achieved by large air cavities in the skull connected to the middle ear and low stiffness of middle ear structures; in the inner ear, the stiffness of round windows and cochlear partitions are key factors. Within the inner ear, the sizes of the helicotrema and cochlear aqueduct are expected to play important roles in shunting low-frequency vibrations away from low-frequency hair-cell sensors in the cochlea. The basilar papilla, the auditory organ in birds, responds to infrasound in some species, and in pigeons, infrasonic-sensitive neurons were traced back to the apical, abneural end of the basilar papilla. Vestibular organs and the paratympanic organ, a hair cell organ outside of the inner ear, are additional untested candidates for infrasound detection in birds. In summary, this review brings together evidence to create a hypothetical framework for infrasonic hearing mechanisms in birds and other animals.

In a highly dynamic airspace, flying animals are predicted to adjust foraging behaviour to variable wind conditions to minimize movement costs. Sexual size dimorphism is widespread in wild animal populations, and for large soaring birds which rely on favourable winds for energy-efficient flight, differences in morphology, wing loading and associated flight capabilities may lead males and females to respond differently to wind. However, the interaction between wind and sex has not been comprehensively tested. We investigated, in a large sexually dimorphic seabird which predominantly uses dynamic soaring flight, whether flight decisions are modulated to variation in winds over extended foraging trips, and whether males and females differ. Using GPS loggers we tracked 385 incubation foraging trips of wandering albatrosses Diomedea exulans, for which males are c. 20% larger than females, from two major populations (Crozet and South Georgia). Hidden Markov models were used to characterize behavioural states-directed flight, area-restricted search (ARS) and resting-and model the probability of transitioning between states in response to wind speed and relative direction, and sex. Wind speed and relative direction were important predictors of state transitioning. Birds were much more likely to take off (i.e. switch from rest to flight) in stronger headwinds, and as wind speeds increased, to be in directed flight rather than ARS. Males from Crozet but not South Georgia experienced stronger winds than females, and males from both populations were more likely to take-off in windier conditions. Albatrosses appear to deploy an energy-saving strategy by modulating taking-off, their most energetically expensive behaviour, to favourable wind conditions. The behaviour of males, which have higher wing loading requiring faster speeds for gliding flight, was influenced to a greater degree by wind than females. As such, our results indicate that variation in flight performance drives sex differences in time-activity budgets and may lead the sexes to exploit regions with different wind regimes.