Sun Compass Research Articles

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.

Sky Compass Orientation in Desert Locusts-Evidence from Field and Laboratory Studies.

Locusts are long-range migratory insects. At high population density, immature animals form marching hopper bands while adults take off and form huge swarms of millions of animals. At low population densities animals are solitarious, but likewise migrate, mostly during the night. Numerous studies aimed at predicting locust infestations showed that migrations both as hopper bands and as adults are largely downwind following seasonal shifts of the tropical convergence zone taking the animals to areas of rainfall. Only a few studies provided evidence for active orientation mechanisms, including the involvement of a sun compass. This scarcity of evidence stands in contrast to recent neurobiological data showing sophisticated neuronal adaptations suited for sky compass navigation. These include a special dorsal eye region with photoreceptors suited to analyze the polarization pattern of the sky and a system of topographically arranged sky compass neurons in the central complex of the brain. Laboratory experiments, moreover, demonstrated polarotaxis in tethered flying animals. The discrepancy of these findings call for more rigorous field studies on active orientation mechanisms in locusts. It remains to be shown how locusts use their internal sky compass during mass migrations and what role it plays to guide solitarious locusts in their natural habitat.

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.

Sun-Compass Orientation in Mediterranean Fish Larvae.

Mortality is very high during the pelagic larval phase of fishes but the factors that determine recruitment success remain unclear and hard to predict. Because of their bipartite life history, larvae of coastal species have to head back to the shore at the end of their pelagic episode, to settle. These settlement-stage larvae are known to display strong sensory and motile abilities, but most work has been focused on tropical, insular environments and on the influence of coast-related cues on orientation. In this study we quantified the in situ orientation behavior of settlement-stage larvae in a temperate region, with a continuous coast and a dominant along-shore current, and inspected both coast-dependent and independent cues. We tested six species: one Pomacentridae, Chromis chromis, and five Sparidae, Boops boops, Diplodus annularis, Oblada melanura, Spicara smaris and Spondyliosoma cantharus. Over 85% of larvae were highly capable of keeping a bearing, which is comparable to the orientation abilities of tropical species. Sun-related cues influenced the precision of bearing-keeping at individual level. Three species, out of the four tested in sufficient numbers, oriented significantly relative to the sun position. These are the first in situ observations demonstrating the use of a sun compass for orientation by wild-caught settlement-stage larvae. This mechanism has potential for large-scale orientation of fish larvae globally.

Electro-optical sun compass with a very high degree of accuracy.

We present a novel electro-optical solar compass that is able to determine the true North direction with an accuracy better than 1/100 of degree, superior to that of any other magnetic or electronic compass that does not resort to differential GPS. The compass has an electronic sensor to determine the line of sight of the Sun and a simple but effective algorithm to calculate the position of the Sun. The excellent results obtained during the experimental tests demonstrate the advantages of this compass, which is also compact and not expensive.

Experience-related reorganization of giant synapses in the lateral complex: Potential role in plasticity of the sky-compass pathway in the desert ant Cataglyphis fortis.

Cataglyphis desert ants undergo an age-related polyethism from interior workers to relatively short-lived foragers with remarkable visual navigation capabilities, predominantly achieved by path integration using a polarized skylight-based sun compass and a stride-integrating odometer. Behavioral and physiological experiments revealed that the polarization (POL) pattern is processed via specialized UV-photoreceptors in the dorsal rim area of the compound eye and POL sensitive optic lobe neurons. Further information about the neuronal substrate for processing of POL information in the ant brain has remained elusive. This work focuses on the lateral complex (LX), known as an important relay station in the insect sky-compass pathway. Neuroanatomical results in Cataglyphis fortis show that LX giant synapses (GS) connect large presynaptic terminals from anterior optic tubercle neurons with postsynaptic GABAergic profiles of tangential neurons innervating the ellipsoid body of the central complex. At the ultrastructural level, the cup-shaped presynaptic structures comprise many active zones contacting numerous small postsynaptic profiles. Three-dimensional quantification demonstrated a significantly higher number of GS (∼ 13%) in foragers compared with interior workers. Light exposure, as opposed to age, was necessary and sufficient to trigger a similar increase in GS numbers. Furthermore, the increase in GS numbers was sensitive to the exclusion of UV light. As previous experiments have demonstrated the importance of the UV spectrum for sky-compass navigation in Cataglyphis, we conclude that plasticity in LX GS may reflect processes involved in the initial calibration of sky-compass neuronal circuits during orientation walks preceding active foraging.

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.

Perceptual strategies of pigeons to detect a rotational centre--a hint for star compass learning?

Birds can rely on a variety of cues for orientation during migration and homing. Celestial rotation provides the key information for the development of a functioning star and/or sun compass. This celestial compass seems to be the primary reference for calibrating the other orientation systems including the magnetic compass. Thus, detection of the celestial rotational axis is crucial for bird orientation. Here, we use operant conditioning to demonstrate that homing pigeons can principally learn to detect a rotational centre in a rotating dot pattern and we examine their behavioural response strategies in a series of experiments. Initially, most pigeons applied a strategy based on local stimulus information such as movement characteristics of single dots. One pigeon seemed to immediately ignore eccentric stationary dots. After special training, all pigeons could shift their attention to more global cues, which implies that pigeons can learn the concept of a rotational axis. In our experiments, the ability to precisely locate the rotational centre was strongly dependent on the rotational velocity of the dot pattern and it crashed at velocities that were still much faster than natural celestial rotation. We therefore suggest that the axis of the very slow, natural, celestial rotation could be perceived by birds through the movement itself, but that a time-delayed pattern comparison should also be considered as a very likely alternative strategy.

Salt concentration and solar orientation in two supralittoral sandhoppers: Talitrus saltator (Montagu) and Talorchestia ugolinii Bellan Santini and Ruffo.

The influence of salt concentration in the seawater on solar orientation in Talitrus saltator and Talorchestia ugolinii was studied in a confined environment (transparent plexiglass bowls). Sodium and calcium concentrations strongly affect both sea-land orientation and the sun compass mechanism in T.saltator, whereas the behaviour of T. ugolinii is less influenced. The absence of Na(+) does not influence the sun compass mechanism, but causes an inversion in the mean direction of orientation in T. saltator. In T. ugolinii, there was no influence on the compass mechanism for solar orientation and no inversion in the directional choice. In the absence of Ca(2+), a photonegative tendency was observed for T saltator together with marked reduction in the capacity to go in any direction. However, the effect of Ca(2+) absence on the orientation capacity of T. saltator is reversible and the orientation capacity can be reduced in a few minutes. The different behaviour of the two species of sandhoppers is discussed.

Compass Orientation During Dispersal of Freshwater Hatchling Snapping Turtles (Chelydra serpentina) and Blanding's Turtles (Emydoidea blandingii)

AbstractFreshwater turtle hatchlings primarily use visual cues for orientation while dispersing from nests; however, hatchlings rapidly develop a relationship between a sun or geomagnetic compass and a dispersal target that allows them to maintain an established direction of movement when target habitats are not visible. We examined dispersal patterns of hatchling snapping turtles (Chelydra serpentina) and Blanding's turtles (Emydoidea blandingii) dispersing in large arenas in a mowed field and in dense corn. The dispersal of three categories of hatchlings were examined: (1) naïve individuals (no previous dispersal experience), (2) arena‐experienced (limited dispersal experience in arenas in natural habitat), and (3) natural‐experienced hatchling Blanding's turtles (captured after extensive experience dispersing W in natural habitats toward wetlands). Experienced hatchlings were assigned to treatments consisting of having a magnet or a non‐magnetic aluminum sham or nothing glued to their anterior carapace before release in the corn arena. Dispersal patterns of naïve hatchlings of both species were strongly directional in the field arena with visible target horizons and primarily random in the corn arena where typical target horizons were blocked. When released in corn, dispersal patterns were similar for arena‐experienced hatchlings with magnets or shams attached and differed from their prior dispersal headings in the field arena as naïve hatchlings. Natural‐experienced hatchling Blanding's turtles with and without magnets were able to accurately maintain their prior headings to the WNW while dispersing in the field or corn arenas (i.e., the presence of a magnet did not disrupt their ability to maintain their prior heading). Based on the assumption that no other type of compass exists in hatchlings, we conclude that they were not using a geomagnetic compass, but by default were using sun compass orientation to maintain dispersal headings in dense corn where no typical target habitats were visible.

Talitrid orientation as bioindicator of shoreline stability: Protected headland-bays versus exposed extended beaches

The behaviour of talitrids, being a local adaptation to beaches, is known to be related to environmental stability. The use of behavioural responses of resident populations as bioindicator of shoreline stability has been tested under various conditions, including after soft and hard engineering actions to stabilise eroded beaches. Port structures likely have impact on sediment longshore transportation and shoreline stability. The question was whether talitrid orientation behaviour could be proposed as bioindicator of impacts also for sandy bays of limited extension and highly used for recreation, such as those in the vicinity of touristic port structures. Orientation experiments were carried out on a set of sandy beaches of different extension and morphology, each of them in the vicinity of a touristic port, across the Mediterranean coasts. The protocol included field orientation tests of populations of talitrids, then analysed in terms of orientation precision seawards (considering sun compass orientation as the most locally adapted behavioural mechanism) in different seasons (before and after the touristic season) and times of day. The populations from more protected (either naturally or artificially) headland-bays showed a higher precision of orientation with respect to the shoreline direction than those from extended beaches, more subject to changes in longshore sedimentary transport as consequence of natural and human activities. The distance from the port and touristic pressure had no influence on talitrid orientation. An important stabilising factor for the sandy beach ecosystems, including talitrid populations and their behavioural adaptation, appeared to be the presence of seagrass banquette. The behavioural data point out that biotic information proceeding from local animal populations linked to beach sediments may complement sedimentology data and allow scaling the impacts occurring on a developed coastline. This becomes particularly relevant when considering interdisciplinary approaches to monitoring strategies.

Long-range seasonal migration in insects: mechanisms, evolutionary drivers and ecological consequences.

Myriad tiny insect species take to the air to engage in windborne migration, but entomology also has its 'charismatic megafauna' of butterflies, large moths, dragonflies and locusts. The spectacular migrations of large day-flying insects have long fascinated humankind, and since the advent of radar entomology much has been revealed about high-altitude night-time insect migrations. Over the last decade, there have been significant advances in insect migration research, which we review here. In particular, we highlight: (1) notable improvements in our understanding of lepidopteran navigation strategies, including the hitherto unsuspected capabilities of high-altitude migrants to select favourable winds and orientate adaptively, (2) progress in unravelling the neuronal mechanisms underlying sun compass orientation and in identifying the genetic complex underpinning key traits associated with migration behaviour and performance in the monarch butterfly, and (3) improvements in our knowledge of the multifaceted interactions between disease agents and insect migrants, in terms of direct effects on migration success and pathogen spread, and indirect effects on the evolution of migratory systems. We conclude by highlighting the progress that can be made through inter-phyla comparisons, and identify future research areas that will enhance our understanding of insect migration strategies within an eco-evolutionary perspective.

Sandhopper orientation under natural conditions: Comparing individual tracks

The analysis of animal movements may help to understand orientation strategies. While there have been many studies on sandhoppers’ orientation mechanisms through the analysis of their orientation angles, no attempts have been made to analyze individual tracks under (varying) natural conditions. The species Talitrus saltator (Montagu, 1808) has the ability to recover the optimal zone of the beach at or below the drift-line and burrow into moist sand when released in the upper beach during the day. On dry sand sandhoppers typically jump and leave tracks; we measured the tracks in relation to the starting point. For each track we calculated: the mean angle of direction, distance covered from the starting point, number of jumps, number of effective turnings, rectilinearity and efficiency (how well the track was directed to the goal). We proposed a classification of the tracks based on both rectilinearity and efficiency. Freshly collected adult individuals from the population of San Rossore beach (Pisa, Italy) were compared to laboratory-born ones so as to highlight eventual differences related to experience. Most of the wild individuals made tracks with high rectilinearity and efficiency. This good orientation suggests that these individuals had developed experience of their beach rapidly recovering the optimal zone. Laboratory-born individuals showed a higher scatter in orientation and winding tracks. The factors that influenced the individuals during their movements could also be inferred by the track course. In addition to the sun azimuth (sun compass), wind direction appeared to be a major factor influencing orientation. The individuals released with onshore winds were more efficiently oriented seawards than those released with winds from other directions.

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.

Reply to Cheung et al.: The cognitive map hypothesis remains the best interpretation of the data in honeybee navigation.

Cheung et al. (1) criticize two points of our study, both of which are unfounded. The first is that general anesthesia is not shifting the clock controlling sun compass orientation in bees. This is clearly wrong. We show that sun compass orientation and food anticipatory behavior are systematically shifted by anesthesia. This effect results from anesthesia shifting the underlying molecular circadian clock of the bee (2).

Seasonal variation in the orientation of Talitrus saltator on a Mediterranean sandy beach: an ecological interpretation

The amphipod Talitrus saltator (Montagu 1808), diffused on the Mediterranean and Eastern Atlantic coasts, displays physiological and behavioural adaptations to life on sandy beaches. To avoid dehydration, sandhoppers burrow in moist sand near the water’s edge during the day in the warmest seasons. When displaced, they can navigate to this safe zone using a sun compass and several additional mechanisms, both universal and local, an adaptive behaviour named ‘zonal recovery’. In this study, we analysed the effects of several variables on the talitrids’ orientation behaviour to highlight the relevance of the local cues and analyse the behavioural variation with relation to the ecology of sandy beaches. In different seasons for 2 years, orientation experiments were made on T. saltator sub-populations, at three sites of an extended sandy beach, differing in shoreline sedimentary dynamics; the main environmental, climatic and individual variables known to influence talitrid orientation were registered during each experimental session. The statistics of circular distributions were calculated and a multiple regression analysis adapted to angular data was performed, to highlight the scaling triggered by environmental conditions. The results showed that seasonal climatic variables played a primary role, adaptively modifying the sandhoppers’ behaviour. A significant interaction with the site (the chosen sites differed for sedimentary dynamics) was observed as well. A high behavioural plasticity appears to guarantee to T. saltator a good adaptation (both as abundance and geographical spreading) to life on sandy beaches, which are notably unstable environments.

Design of a device for sky light polarization measurements.

Sky polarization patterns can be used both as indicators of atmospheric turbidity and as a sun compass for navigation. The objective of this study is to improve the precision of sky light polarization measurements by optimal design of the device used. The central part of the system is composed of a Charge Coupled Device (CCD) camera; a fish-eye lens and a linear polarizer. Algorithms for estimating parameters of the polarized light based on three images are derived and the optimal alignments of the polarizer are analyzed. The least-squares estimation is introduced for sky light polarization pattern measurement. The polarization patterns of sky light are obtained using the designed system and they follow almost the same patterns of the single-scattering Rayleigh model. Deviations of polarization angles between observation and the theory are analyzed. The largest deviations occur near the sun and anti-sun directions. Ninety percent of the deviations are less than 5° and 40% percent of them are less than 1°. The deviations decrease evidently as the degree of polarization increases. It also shows that the polarization pattern of the cloudy sky is almost identical as in the blue sky.

Transfer of directional information between the polarization compass and the sun compass in desert ants

Desert ants, Cataglyphis fortis, perform large foraging excursions during which they continuously compute a home vector that allows them to return to the nest on the shortest way. This type of navigation, termed path integration, needs a compass system and an odometer. Ants use several cues to determine their walking direction, two of the most important ones being the sun position and the polarization pattern of the sky. We tested whether an information transfer is possible from one compass system to the other, which depend on different anatomical substrates. Since the sky's polarization pattern is detected by UV-photoreceptors located in the dorsal rim area (DRA), we used an orange Perspex filter that eliminated the UV part of the spectrum to prevent the use of the polarization compass. The use of the sun compass could be excluded by appropriate screens. In the critical tests the ants had learned a nest-feeder direction with e.g. the sun compass only, and were later tested with the polarization compass, or vice versa. The results show that a transfer is possible in both directions.

Erratum to: Interactions of the polarization and the sun compass in path integration of desert ants

Erratum to: Interactions of the polarization and the sun compass in path integration of desert ants