Time-compensated Sun Compass Research Articles

Drosophila require both green and UV wavelengths for sun orientation but lack a time-compensated sun compass.

Celestial orientation and navigation are performed by many organisms in contexts as diverse as migration, nest finding and straight-line orientation. The vinegar fly, Drosophila melanogaster, performs menotaxis in response to celestial cues during tethered flight and can disperse more than 10 km under field conditions. However, we still do not understand how spectral components of celestial cues and pauses in flight impact heading direction in flies. To assess individual heading, we began by testing flies in a rotating tether arena using a single green LED as a stimulus. We found that flies robustly perform menotaxis and fly straight for at least 20 min. Flies maintain their preferred heading directions after experiencing a period of darkness or stopping flight, even up to 2 h, but reset their heading when the LED changes position, suggesting that flies do not treat this stimulus as the sun. Next, we assessed the flies' responses to a UV spot alone or a paired UV-green stimulus - two dots situated 180deg apart to simulate the solar and antisolar hemispheres. We found that flies respond to UV much as they do to green light; however, when the stimuli are paired, flies adjust for sudden 90deg movements, performing sun orientation. Lastly, we found no evidence of a time-compensated sun compass when we moved the paired stimuli at 15degh-1 for 6 h. This study demonstrates that wavelength influences how flies respond to visual cues during flight, shaping the interpretation of visual information to execute an appropriate behavioral response.

ECR Spotlight – Haneal Pae

ECR Spotlight is a series of interviews with early-career authors from a selection of papers published in Journal of Experimental Biology and aims to promote not only the diversity of early-career researchers (ECRs) working in experimental biology but also the huge variety of animals and physiological systems that are essential for the ‘comparative’ approach. Haneal Pae is an author on ‘ Drosophila require both green and UV wavelengths for sun orientation but lack a time-compensated sun compass’, published in JEB. Haneal is a PhD student in the lab of Ysabel Giraldo at University of California, Riverside, USA, investigating how sensory information is integrated and processed in the nervous system and influences Drosophila orientation during flight.

Time-compensated sun compass in juvenile sprat (Sprattus sprattus) reveals the onset of migratory readiness.

Sprat (Sprattus sprattus) is one of the most commercially exploited fish species in the Baltic Sea and expresses a pronounced seasonal migration pattern. Spawning takes place, among other places, in the Kiel Bight and Kiel Fjord in early summer. Juvenile sprat leave the nursery areas in late summer/early autumn to move to their feeding and overwintering grounds. What kind of orientation mechanisms sprat use for migration is not known yet. This study shows that juvenile sprat can use a time-compensated sun compass, heading towards the northeast, in the direction of their proposed overwintering grounds in Bornholm Basin. The sprats tested at the end of August oriented themselves in the predicted direction, whereas the sprats tested at the beginning of August only showed a random orientation. For the first time, this demonstrates the onset of migratory readiness in juvenile sprat, indicating the preparation for starting their migration.

The efficiency of varying methods and degrees of time compensation for the solar azimuth.

Daytime migrants are known to orientate using the position of the sun, compensating for its changing position throughout the day with a 'time-compensated sun compass'. This compass has been demonstrated in many migratory species, with various degrees of accuracy for the actual movement of the sun. Here, we present a model for differing levels of compensation for the solar ephemeris that shows that a high degree of efficiency, in terms of distance travelled, can be achieved without full time compensation. In our model, compensating for the sun's position had a diminishing return with an accuracy of 80% leading to only a 2% reduction in distance travelled. We compare various modes of time compensation-full, partial, time averaged and step-revealing their directional efficiency in terms of distance travelled under an autumn migration scenario. We find that the benefit of time compensation varies with latitude, with time averaging performing very well, especially at all high latitudes, but step compensation performing better at very low latitudes. Importantly, even rudimentary adjustment can dramatically increase the efficiency of migration, which suggests an easy pathway for the independent evolution of time compensation.

Juvenile Atlantic herring (Clupea harengus) use a time-compensated sun compass for orientation.

Atlantic herring (Clupea harengus), an ecologically and economically important species in the northern hemisphere, shows pronounced seasonal migratory behaviour. To follow distinctive migration patterns over hundreds of kilometers between feeding, overwintering and spawning grounds, they are probably guided by orientation mechanisms. We tested whether juvenile spring-spawning Atlantic herring, caught in the western Baltic, use a sun compass for orientation just before they start leaving their hatching area. Fish were randomly divided into two groups, one of them clock-shifted 6 h backwards, to investigate whether they shift their orientation direction accordingly. Individual fish were placed in a circular bowl and their orientation was tested multiple times with the sun as a sole visual orientational cue. Our results show for the first time that juvenile Atlantic herring use a time-compensated sun compass during their migration. Their swimming direction was impaired, but still present, even when the sky was very cloudy, indicating additional orientation capabilities.

Oriented migratory flight at night: Consequences of nighttime light pollution for monarch butterflies

SummaryWe show that light trespass—a form of nighttime light pollution (NLP)—elicits normal daytime clock-mediated migratory behavior in fall monarch butterflies during their night-cycle. In controlled indoor flight simulator studies isolating the role of NLP on the expression of oriented migratory flight using a time-compensated sun compass,a full-spectrum light source consistent with lights used outdoors at night by the public,triggered proper fall directional flight at night in monarchs. Monarchs remained quiescent when initially placed in the flight simulator in the dark, but flight was immediately triggered when our light source was turned on. This nighttime behavior was identical to that seen in outdoor free-flying fall conspecifics during the day. The light source provided directional cues equivalent to those provided by the sun and could either phase-advance or phase-delay monarchs. Our study highlights the negative consequences of NLP on diurnal animals, especially those that rely on clock-mediated behavior.

Stimulus-dependent orientation strategies in monarch butterflies.

ABSTRACTInsects 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, 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 whether 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 with a simulated sun stimulus, the butterflies switched their behavior and exhibited compass orientation. Taken together, our data show that monarch butterflies rely on and switch between different orientation modes, allowing the animal to adjust orientation to its actual behavioral demands.

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.

Finding Nemo\u2019s 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.

Circadian plasticity in honey bees

Circadian rhythms of about a day are ubiquitous in animals and considered functionally significant. Honey bees show remarkable circadian plasticity that is related to the complex social organization of their societies. Forager bees show robust circadian rhythms that support time-compensated sun-compass navigation, dance communication and timing visits to flowers. Nest-dwelling nurse bees care for the young brood around the clock. Here, we review our current understanding of the molecular and neuroanatomical mechanisms underlying this remarkable natural plasticity in circadian rhythms.

Use of sun compass orientation during natal dispersal in Blanding’s turtles: in situ field experiments with clock-shifting and disruption of magnetoreception

When hatchling freshwater turtles emerge from nests and first experience environmental stimuli, they primarily use visual cues to disperse toward nearby open horizons or far dark horizons. Within hours, hatchling Blanding’s turtles (Emydoidea blandingii) develop compass mechanisms to maintain their headings when the initial dispersal targets become invisible. We captured hatchling Blanding’s turtles during dispersal in natural habitat, attached a magnetic or non-magnet disk to each turtle, translocated them into an arena in a visually uniform field of corn, and measured their compass orientation (heading). Hatchlings from the magnet and no-magnet groups were evenly divided into two environmental chambers (6-h clock-shift or non-clock-shift) to create four experimental treatments. After 5 to 11 days hatchlings were re-released in the arena. If hatchlings used a time-compensated sun compass, then clock-shifting would cause a ~90° change in heading. If they used a geomagnetic compass, disruption of magnetoreception would cause wandering. If both compasses were used simultaneously or sequentially, we predicted a range of outcomes. All four treatment groups dispersed directionally during both trials, maintaining their prior headings in natural habitat except for the clock-shift treatment which changed heading ~90° as predicted. The ability of hatchlings to maintain prior headings despite the disruption of geomagnetism supports the absence, inactivity, or disregard of a geomagnetic compass. Only a time-compensated sun compass coupled with an internal clock was necessary and sufficient for hatchlings to maintain compass headings during natal dispersal when relocated from natural prairie habitat to a monoculture habitat with a relatively uniform visual horizon. Individuals moving long distances (e.g., migrating birds or dispersing salamanders) often maintain their movement headings using compass orientation (i.e., a geomagnetic or time-compensated sun compass). When hatchling freshwater turtles emerge from underground terrestrial nests they initiate dispersal in search of wetlands primarily based on visual horizon cues. Because such cues often become obscured by uneven terrain or dense vegetation and because straight-line travel is more efficient and less risky, hatchlings soon develop a mechanism of compass orientation to maintain their dispersal headings. We disrupted their ability to use magnetoreception by attaching magnets to their shells, manipulated their sense of time-of-day with clock-shifting, and then monitored their dispersal in a visually uniform field of mature corn. Our results demonstrated that a sun compass was necessary and sufficient for hatchlings with dispersal experience to maintain their dispersal headings when natural environmental cues were not visible.

In Situ Clock Shift Reveals that the Sun Compass Contributes to Orientation in a Pelagic Seabird

Compass orientation is central to the control of animal movement from the scale of local food-caching movements around a familiar area in parids [1] and corvids [2, 3] to the first autumn vector navigation of songbirds embarking on long-distance migration [4-6]. In the study of diurnal birds, where the homing pigeon, Columba livia, has been the main model, a time-compensated sun compass [7] is central to the two-step map-and-compass process of navigation from unfamiliar places, as well as guiding movement via a representation of familiar area landmarks [8-12]. However, its use by an actively navigating wild bird is yet to be shown. By phase shifting an animal's endogenous clock, known as clock-shifting [13-15], sun-compass use can be demonstrated when the animal incorrectly consults the sun's azimuthal position while homing after experimental displacement [15-17]. By applying clock-shift techniques at the nest of a wild bird during natural incubation, we show here that an oceanic navigator-the Manx shearwater, Puffinus puffinus-incorporates information from a time-compensated sun compass during homeward guidance to the breeding colony after displacement. Consistently with homing pigeons navigating within their familiar area [8, 9, 11, 18], we find that the effect of clock shift, while statistically robust, is partial in nature, possibly indicating the incorporation of guidance from landmarks into movement decisions.

Using Online Active-Learning Techniques to Convey Time Compensated Sun Compass Orientation in the Eastern North American Monarch.

A common tool that animals use to navigate in a constant direction is known as “time compensated sun compass orientation.” This is a process by which animals use the position of the sun along with information from their internal circadian clocks to determine and maintain a directional heading. Many circadian scientists and educators use this process as an example of how the internal circadian clock can directly influence animal behavior. However, many students have difficulty grasping this biological process due to its multivariable nature. We have created an online module that uses the principles of active learning to facilitate student comprehension of this process. Our module contains instructional videos, practice problems and an interactive diagram. We implemented the module in an undergraduate biological clocks class at Vanderbilt University, where its use significantly improved students’ understanding of time compensated sun compass orientation as well as their ability to solve complex problems involving principles associated with this process.

Evidence for discrete solar and lunar orientation mechanisms in the beach amphipod, Talitrus saltator Montagu (Crustacea, Amphipoda)

Animals that use astronomical cues to orientate must make continuous adjustment to account for temporal changes in azimuth caused by Earth’s rotation. For example, the Monarch butterfly possesses a time-compensated sun compass dependent upon a circadian clock in the antennae. The amphipod Talitrus saltator possesses both a sun compass and a moon compass. We reasoned that the time-compensated compass mechanism that enables solar orientation of T. saltator is located in the antennae, as is the case for Monarch butterflies. We examined activity rhythms and orientation of sandhoppers with antennae surgically removed, or unilaterally occluded with black paint. Removing or painting the antennae did not affect daily activity rhythms or competence to orientate using the sun. However, when tested at night these animals were unable to orientate correctly to the moon. We subsequently measured circadian gene expression in the antennae and brain of T. saltator and show the clock genes period and cryptochrome 2 are rhythmically expressed in both tissues, reminiscent of other arthropods known to possess antennal clocks. Together, our behavioural and molecular data suggest that, T. saltator has anatomically discrete lunar and solar orientation apparatus; a sun compass, likely located in the brain and a moon compass in the antennae.

Neural Integration Underlying a Time-Compensated Sun Compass in the Migratory Monarch Butterfly.

Migrating eastern North American monarch butterflies use a time-compensated sun compass to adjust their flight to the southwest direction. Although the antennal genetic circadian clock and the azimuth of the sun are instrumental for proper function of the compass, it is unclear how these signals are represented on a neuronal level and how they are integrated to produce flight control. To address these questions, we constructed a receptive field model of the compound eye that encodes the solar azimuth. We then derived a neural circuit model that integrates azimuthal and circadian signals to correct flight direction. The model demonstrates an integration mechanism, which produces robust trajectories reaching the southwest regardless of the time of day and includes a configuration for remigration. Comparison of model simulations with flight trajectories of butterflies in a flight simulator shows analogous behaviors and affirms the prediction that midday is the optimal time for migratory flight.

Assessing vector navigation in long-distance migrating birds

Birds migrating between distant locations regularly perform long continuous flights lasting several days. What compass mechanism they use is still a mystery. Here, we use a novel approach, applying an individual-based model, taking compass mechanisms based on celestial and geomagnetic information and wind into account simultaneously, to investigate what compass mechanism likely is used during long continuous flights and how wind drift or compensation affects the resulting tracks. We found that for the 6 cases of long continuous migration flights, the magnetoclinic route could best explain the route selection in all except one case compared with the alternative compass mechanisms. A flight strategy correcting for wind drift resulted most often in routes ending up closest to the predicted destinations. In only half of the cases could a time-compensated sun compass explain the migration routes observed with sufficient precision. Migration from Europe to the Siberian tundra was especially challenging to explain by one compass mechanism alone, suggesting a more complex navigation strategy. Our results speak in favor of a magnetic compass based on the angle of inclination used by birds during continuous long-distance migration flights, but also a capacity to detect and correct for drift caused by winds along the route.

Neurobiology of Monarch Butterfly Migration.

Studies of the migration of the eastern North American monarch butterfly (Danaus plexippus) have revealed mechanisms behind its navigation. The main orientation mechanism uses a time-compensated sun compass during both the migration south and the remigration north. Daylight cues, such as the sun itself and polarized light, are processed through both eyes and integrated through intricate circuitry in the brain's central complex, the presumed site of the sun compass. Monarch circadian clocks have a distinct molecular mechanism, and those that reside in the antennae provide time compensation. Recent evidence shows that migrants can also use a light-dependent inclination magnetic compass for orientation in the absence of directional daylight cues. The monarch genome has been sequenced, and genetic strategies using nuclease-based technologies have been developed to edit specific genes. The monarch butterfly has emerged as a model system to study the neural, molecular, and genetic basis of long-distance animal migration.

Cues indicating location in pigeon navigation

Domesticated Rock Pigeons (Columba livia f. domestica) have been selected for returning home after being displaced. They appear to use many of the physical cue sources available in the natural environment for Map-and-Compass navigation. Two compass mechanisms that have been well documented in pigeons are a time-compensated sun compass and a magnetic inclination compass. Location-finding, or map, mechanisms have been more elusive. Visual landmarks, magnetic fields, odors, gravity and now also infrasound have been proposed as sources of information on location. Even in highly familiar locations, pigeons appear to neither use nor need landmarks and can even return to the loft while wearing frosted lenses. Direct and indirect evidence indicates magnetic field information influences pigeon navigation in ways that are consistent with magnetic map components. The role of odors is unclear; it might be motivational in nature rather than navigational. The influence of gravity must be further analyzed. Experiments with infrasound have been interpreted in the sense that they provide information on the home direction, but this hypothesis is inconsistent with the Map-and-Compass Model. All these factors appear to be components of a multifactorial system, with the pigeons being opportunistic, preferring those cues that prove most suitable in their home region. This has made understanding the roles of individual cues challenging.

The sun compass revisited

Many animals, and birds in particular, are thought to use directional information from the sun in the form of a time-compensated sun compass, with predictably deviated orientation under clock shift being regarded as the litmus test of this. We suggest that this paradigm obscures a number of other ways in which solar-derived information could be important in animal orientation. We distinguish between the known use of the sun's azimuth to provide absolute geographical direction (compass mechanism) and its possible use to detect changes in heading (heading indicator mechanism). Just as in an aircraft, these two kinds of information may be provided by separate mechanisms and used for different functions, for example for navigation versus steering. We also argue that although a solar compass must be time-referenced to account for the sun's apparent diurnal movement, this need not entail full time compensation. This is because animals might also use time-dependent solar information in an associatively acquired, and hence time-limited, way. Furthermore, we show that a solar heading indicator, when used on a sufficiently short timescale, need not require time compensation at all. Finally, we suggest that solar-derived cues, such as shadows, could also be involved in navigation in ways that depend explicitly upon position, and are therefore not strictly compass-related. This could include giving directionality to landmarks, or acting as time-dependent landmarks involved in place recognition. We conclude that clock shift experiments alone are neither necessary nor sufficient to identify the occurrence of all conceivable uses of solar information in animal orientation, so that a predictable response to clock shift should not be regarded as an acid test of the use of solar information in navigation.

A magnetic compass aids monarch butterfly migration.

Convincing evidence that migrant monarch butterflies (Danaus plexippus) use a magnetic compass to aid their fall migration has been lacking from the spectacular navigational capabilities of this species. Here we use flight simulator studies to show that migrants indeed possess an inclination magnetic compass to help direct their flight equatorward in the fall. The use of this inclination compass is light-dependent utilizing ultraviolet-A/blue light between 380 and 420 nm. Notably, the significance of light <420 nm for inclination compass function was not considered in previous monarch studies. The antennae are important for the inclination compass because they appear to contain light-sensitive magnetosensors. For migratory monarchs, the inclination compass may serve as an important orientation mechanism when directional daylight cues are unavailable and may also augment time-compensated sun compass orientation for appropriate directionality throughout the migration.