Self-correcting Sun Compass, Spherical Geometry and Cue-transfers Predict Naïve Migratory Performance

Migratory orientation of many animals is inheritable, enabling naïve migrants to reach remote destinations independently following stepwise (often, nightly) geomagnetic or celestial cues. Which if any such “compass courses” can explain narrow-front trans-continental routes remains unresolved, and evident error-corrections by naïve migrants remain unexplained. We assessed robustness to errors among airborne compass courses and quantified inaugural migration performance globally, accounting for cue transfers (e.g., sun to star compass), in-flight cue maintenance, and previously-overlooked spherical-geometry (longitude) effects. We found (i) sun-compass courses partially self-correct, making them most robust between flight-steps, (ii) within nocturnal flight-steps, geomagnetic or star-compass headings outperform cue-transferred sun-compass steps, (iii) across diverse airborne migration routes, the relative favourability of sun-compass over other courses increases with increasing goal-area, required flight steps and a spherical-geometry factor. Our results can explain enhanced naïve migrant performance, observed diversity in compass-cue hierarchies, and sun-compass orientation being key to many long-distance inaugural migrations.

Stimulus-dependent orientation strategies in monarch butterflies

Insects are well-known for their ability to keep track of their heading direction based on a combination of skylight cues and visual landmarks. This allows them to navigate back to their nest, disperse throughout unfamiliar environments, as well as migrate over large distances between their breeding and non-breeding habitats. The monarch butterfly (Danaus plexippus) for instance is known for its annual southward migration from North America to certain trees in Central Mexico. To maintain a constant flight route, these butterflies use a time-compensated sun compass for orientation which is processed in a region in the brain, termed the central complex. However, to successfully complete their journey, the butterflies' brain must generate a multitude of orientation strategies, allowing them to dynamically switch from sun-compass orientation to a tactic behavior toward a certain target. To study if monarch butterflies exhibit different orientation modes and if they can switch between them, we observed the orientation behavior of tethered flying butterflies in a flight simulator while presenting different visual cues to them. We found that the butterflies' behavior depended on the presented visual stimulus. Thus, while a dark stripe was used for flight stabilization, a bright stripe was fixated by the butterflies in their frontal visual field. If we replaced a bright stripe by a simulated sun stimulus, the butterflies switched their orientation behavior and exhibited compass orientation. Taken together, our data show that monarch butterflies rely on and switch between different orientation modes, allowing them to adjust orientation to the actual behavioral demands of the animal.

Hoverflies use a time-compensated sun compass to orientate during autumn migration

The sun is the most reliable celestial cue for orientation available to daytime migrants. It is widely assumed that diurnal migratory insects use a ‘time-compensated sun compass’ to adjust for the changing position of the sun throughout the day, as demonstrated in some butterfly species. The mechanisms used by other groups of diurnal insect migrants remain to be elucidated. Migratory species of hoverflies (Diptera: Syrphidae) are one of the most abundant and beneficial groups of diurnal migrants, providing multiple ecosystem services and undergoing directed seasonal movements throughout much of the temperate zone. To identify the hoverfly navigational strategy, a flight simulator was used to measure orientation responses of the hoverflies Scaeva pyrastri and Scaeva selenitica to celestial cues during their autumn migration. Hoverflies oriented southwards when they could see the sun and shifted this orientation westward following a 6 h advance of their circadian clocks. Our results demonstrate the use of a time-compensated sun compass as the primary navigational mechanism, consistent with field observations that hoverfly migration occurs predominately under clear and sunny conditions.

Orientation cues and mechanisms used during avian navigation: A review

The navigational systems of different animal species are by a wide margin less notable as compared to birds. Humans have been interested in how migratory birds discover their way more than thousands of miles for quite a long time. This review summarizes the cues and compass mechanisms applied in orientation and navigation by non-migrants, diurnal and nocturnal migrants. The magnetic compass, landmarks, olfactory, and memory of spatial cues en route were utilized in homing and migration. The equivalent is valid for the sun compass despite the fact that its job during migration might be undeniably less significant than commonly presumed. Stellar compass and celestial rotation, as a result of their nighttime accessibility, appear to influence the direction of nighttime migrants during the course of migration. The celestial cues go through notable changes because of the latitude shift during bird migration. Sunset cues alter their location with seasons and latitudes. The recognizable stars lose height and lastly vanish underneath the horizon, whereas new stars show up. These new ones must be calibrated. As celestial rotation not imparting a reference, it is not unexpected that the magnetic compass turns into the main cue that controls the directional importance of stars and sunset cues. Field studies have revealed that, in certain species, a considerable extent of individuals get back to similar breeding, overwintering, and stopover areas in progressive years. This review proposes that migratory birds have advanced uncommon cognitive capacities that empower them to achieve these accomplishments.

Finding Nemo’s clock reveals switch from nocturnal to diurnal activity

Timing mechanisms play a key role in the biology of coral reef fish. Typically, fish larvae leave their reef after hatching, stay for a period in the open ocean before returning to the reef for settlement. During this dispersal, larvae use a time-compensated sun compass for orientation. However, the timing of settlement and how coral reef fish keep track of time via endogenous timing mechanisms is poorly understood. Here, we have studied the behavioural and genetic basis of diel rhythms in the clown anemonefish Amphiprion ocellaris. We document a behavioural shift from nocturnal larvae to diurnal adults, while juveniles show an intermediate pattern of activity which potentially indicates flexibility in the timing of settlement on a host anemone. qRTPCR analysis of six core circadian clock genes (bmal1, clocka, cry1b, per1b, per2, per3) reveals rhythmic gene expression patterns that are comparable in larvae and juveniles, and so do not reflect the corresponding activity changes. By establishing an embryonic cell line, we demonstrate that clown anemonefish possess an endogenous clock with similar properties to that of the zebrafish circadian clock. Furthermore, our study provides a first basis to study the multi-layered interaction of clocks from fish, anemones and their zooxanthellae endosymbionts.

Sun compass neurons are tuned to migratory orientation in monarch butterflies

Every autumn, monarch butterflies migrate from North America to their overwintering sites in Central Mexico. To maintain their southward direction, these butterflies rely on celestial cues as orientation references. The position of the sun combined with additional skylight cues are integrated in the central complex, a region in the butterfly's brain that acts as an internal compass. However, the central complex does not solely guide the butterflies on their migration but also helps monarchs in their non-migratory form manoeuvre on foraging trips through their habitat. By comparing the activity of input neurons of the central complex between migratory and non-migratory butterflies, we investigated how a different lifestyle affects the coding of orientation information in the brain. During recording, we presented the animals with different simulated celestial cues and found that the encoding of the sun was narrower in migratory compared to non-migratory butterflies. This feature might reflect the need of the migratory monarchs to rely on a precise sun compass to keep their direction during their journey. Taken together, our study sheds light on the neural coding of celestial cues and provides insights into how a compass is adapted in migratory animals to successfully steer them to their destination.

Ontogeny of the star compass in birds: pied flycatchers (Ficedula hypoleuca) can establish the star compass in spring

ABSTRACTThe star compass of birds, like the sun compass, is not innate. To possess either of them, birds have to observe the rotating sky and determine its centre of rotation (in the case of the star compass) or the sun's movement (for the sun compass). Young birds are believed to learn how to use the star compass before their first migration, even though the evidence of this is lacking. Here, we tested whether hand-raised Pied flycatchers (Ficedula hypoleuca) that had not established the star compass prior to their first autumn migration can gain it later in their ontogeny, in spring. We also attempted to examine whether the observation of diurnal celestial cues (the sun and polarized light) prior to autumn migration would affect the process of star compass learning in spring. When tested in the vertical magnetic field under the natural starry sky, the group of birds that observed the stars in spring as the first celestial cues were able to choose the migratory direction. In contrast, the birds that had never seen the stars were not able to use the nightly celestial cues in the vertical magnetic field. However, birds that had seen the daytime celestial cues till autumn and the stars at spring were disoriented, although this might be due to the small sample size. Our data suggest the possibility that the star compass may be learned in spring and emphasize the necessity for further research into the interaction of celestial compasses.

Model and Non-model Insects in Chronobiology

The fruit fly Drosophila melanogaster is an established model organism in chronobiology, because genetic manipulation and breeding in the laboratory are easy. The circadian clock neuroanatomy in D. melanogaster is one of the best-known clock networks in insects and basic circadian behavior has been characterized in detail in this insect. Another model in chronobiology is the honey bee Apis mellifera, of which diurnal foraging behavior has been described already in the early twentieth century. A. mellifera hallmarks the research on the interplay between the clock and sociality and complex behaviors like sun compass navigation and time-place-learning. Nevertheless, there are aspects of clock structure and function, like for example the role of the clock in photoperiodism and diapause, which can be only insufficiently investigated in these two models. Unlike high-latitude flies such as Chymomyza costata or D. ezoana, cosmopolitan D. melanogaster flies do not display a photoperiodic diapause. Similarly, A. mellifera bees do not go into “real” diapause, but most solitary bee species exhibit an obligatory diapause. Furthermore, sociality evolved in different Hymenoptera independently, wherefore it might be misleading to study the social clock only in one social insect. Consequently, additional research on non-model insects is required to understand the circadian clock in Diptera and Hymenoptera. In this review, we introduce the two chronobiology model insects D. melanogaster and A. mellifera, compare them with other insects and show their advantages and limitations as general models for insect circadian clocks.

Matched-filter coding of sky polarization results in an internal sun compass in the brain of the desert locust

Many animals use celestial cues for spatial orientation. These include the sun and, in insects, the polarization pattern of the sky, which depends on the position of the sun. The central complex in the insect brain plays a key role in spatial orientation. In desert locusts, the angle of polarized light in the zenith above the animal and the direction of a simulated sun are represented in a compass-like fashion in the central complex, but how both compasses fit together for a unified representation of external space remained unclear. To address this question, we analyzed the sensitivity of intracellularly recorded central-complex neurons to the angle of polarized light presented from up to 33 positions in the animal’s dorsal visual field and injected Neurobiotin tracer for cell identification. Neurons were polarization sensitive in large parts of the virtual sky that in some cells extended to the horizon in all directions. Neurons, moreover, were tuned to spatial patterns of polarization angles that matched the sky polarization pattern of particular sun positions. The horizontal components of these calculated solar positions were topographically encoded in the protocerebral bridge of the central complex covering 360° of space. This whole-sky polarization compass does not support the earlier reported polarization compass based on stimulation from a small spot above the animal but coincides well with the previously demonstrated direct sun compass based on unpolarized light stimulation. Therefore, direct sunlight and whole-sky polarization complement each other for robust head direction coding in the locust central complex.

Is There Visual Lateralisation of the Sun Compass in Homing Pigeons?

Functional lateralisation in the avian visual system can be easily studied by testing monocularly occluded birds. The sun compass is a critical source of navigational information in birds, but studies of visual asymmetry have focussed on cues in a laboratory rather than a natural setting. We investigate functional lateralisation of sun compass use in the visual system of homing pigeons trained to locate food in an outdoor octagonal arena, with a coloured beacon in each sector and a view of the sun. The arena was rotated to introduce a cue conflict, and the experimental groups, a binocular treatment and two monocular treatments, were tested for their directional choice. We found no significant difference in test orientation between the treatments, with all groups showing evidence of both sun compass and beacon use, suggesting no complete functional lateralisation of sun compass use within the visual system. However, reduced directional consistency of binocular vs. monocular birds may reveal a conflict between the two hemispheres in a cue conflict condition. Birds using the right hemisphere were more likely to choose the intermediate sector between the training sector and the shifted training beacon, suggesting a possible asymmetry in favour of the left eye/right hemisphere (LE/RH) when integrating different cues.