Hippocampal lesions do not impair the geomagnetic orientation of migratory savannah sparrows

The avian hippocampal formation is known to participate in naturally occurring spatial behavior such as homing in pigeons and cache recovery in food storing passerines, but its participation in the often spectacular migrations of birds remains uncertain. As a first investigation into the possible role of hippocampal formation in migration, the effect of hippocampal formation lesions on the geomagnetic migratory orientation of Savannah sparrows was examined. When tested indoors, hippocampal formation-lesioned sparrows were able to orient in an appropriate migratory direction indicating no necessary role for hippocampal formation in geomagnetic migratory orientation. However, hippocampal formation-lesioned birds displayed significantly less migratory (nocturnal) activity, a result that inspires further study. Accepted: 25 August 1999     

Biogenic magnetite as a basis for magnetic field detection in animals

Bacteria, sharks, honey bees, and homing pigeons as well as other organisms seem to detect the direction of the earth's magnetic field. Indirect but reproducible evidence suggests that the bees and birds can also respond to very minute changes in its intensity. The mechanisms behind this sensitivity are not known. Naturally magnetic, biologically precipitated magnetite (Fe₃O₄) has been found in chitons, magnetotactic bacteria, honey bees, homing pigeons, and dolphins. Its mineralization in localized areas may be associated with the ability of these animals to respond to the direction and intensity of the earth's magnetic field. The presence of large numbers (～10⁸) of superparamagnetic magnetite crystals in honey bees and similar numbers of single-domain magnetite grains in pigeons suggests that there may be at least two basic types of ferrimagnetic magnetoreceptive organelles. Theoretical calculations show that ferrimagnetic organs using either type of grain when integrated by the nervous system are capable of accounting for even the most extreme magnetic field sensitivities reported. Indirect evidence suggests that organic magnetite may be a common biological component, and may account for the results of numerous high field and electromagnetic experiments on animals.     

Superparamagnetic Magnetite in the Upper Beak Tissue of Homing Pigeons

Homing pigeons have been subject of various studies trying to detect magnetic material which might be involved in magnetic field perception. Here we focus on the upper-beak skin of homing pigeons, a region that has previously been shown to contain nerves sensitive to changes of the ambient magnetic field. We localized Fe³⁺ concentrations in the subcutis and identified the material by transmission electronmicroscopy (TEM) as aggregates of magnetite nanocrystals (with grain sizes between 1 and 5 nm). The particles form clusters of 1–3 m diameter, which are arranged in distinct coherent elongated structures, associated with nervous tissue and located between fat cells. Complementary low-temperature magnetic measurements confirm the microscopic observations of fine-grained superparamagnetic particles in the tissue. Neither electron-microscopic nor magnetic measurements revealed any single-domain magnetite in the upper-beak skin tissue.     

Homing pigeons as a model for avian navigation?

The findings on the navigational mechanisms of homing pigeons and the available data on those of wild birds, in particular migrants, are compared. There are important parallels in the use of the magnetic field and the sun for directional orientation. Also the findings on the navigational ‘map’, its preferred use by experienced birds and the strategy of using route information to acquire the necessary knowledge to establish the ‘map’, obtained in pigeons studies, can probably be generalized to wild birds and migrants in their home region. It seems that birds share a common navigational system. Special development of migratory birds, however, is the innate migration program that enables young first‐time migrants to reach their still unknown wintering area.     

Pineal Body and Magnetic Sensitivity: Homing in Pinealectomized Pigeons under Overcast Skies

Since birds use the earth's magnetic field for compass orientation when astronomical cues are lacking and it has recently been suggested that the pineal body is part of their magnetic compass, test releases have been performed in overcast conditions with pigeons deprived of the pineal body. On the whole, both experimental and control birds were capable of homeward orientation, though the bearings of experimental were rather more scattered. No differences in homing speed or success were recorded. Thus, the pineal body does not appear to play an important role in the homing of pigeons.     

The magnetite-based receptors in the beak of birds and their role in avian navigation

Iron-rich structures have been described in the beak of homing pigeons, chickens and several species of migratory birds and interpreted as magnetoreceptors. Here, we will briefly review findings associated with these receptors that throw light on their nature, their function and their role in avian navigation. Electrophysiological recordings from the ophthalmic nerve, behavioral studies and a ZENK-study indicate that the trigeminal system, the nerves innervating the beak, mediate information on magnetic changes, with the electrophysiological study suggesting that these are changes in intensity. Behavioral studies support the involvement of magnetite and the trigeminal system in magnetoreception, but clearly show that the inclination compass normally used by birds represents a separate system. However, if this compass is disrupted by certain light conditions, migrating birds show ‘fixed direction’ responses to the magnetic field, which originate in the receptors in the beak. Together, these findings point out that there are magnetite-based magnetoreceptors located in the upper beak close to the skin. Their natural function appears to be recording magnetic intensity and thus providing one component of the multi-factorial ‘navigational map’ of birds.     

Magnetic pulse affects a putative magnetoreceptor mechanism

Clusters of superparamagnetic (SP) magnetite crystals have recently been identified in free nerve endings in the upper-beak skin of homing pigeons and are interpreted as being part of a putative magnetoreceptor system. Motivated by these findings, we developed a physical model that accurately predicts the dynamics of interacting SP clusters in a magnetic field. The main predictions are: 1), under a magnetic field, a group of SP clusters self-assembles into a chain-like structure that behaves like a compass needle under slowly rotating fields; 2), in a frequently changing field as encountered by a moving bird, a stacked chain is a structurally more stable configuration than a single chain; 3), chain-like structures of SP clusters disrupt under strong fields applied at oblique angles; and 4), reassemble on a timescale of hours to days (assuming a viscosity of the cell plasma eta approximately 1 P). Our results offer a novel mechanism for magnetic field perception and are in agreement with the response of birds observed after magnetic-pulse treatments, which have been conducted in the past to specifically test if ferrimagnetic material is involved in magnetoreception, but which have defied explanation so far. Our theoretical results are supported by experiments on a technical SP model system using a high-speed camera. We also offer new predictions that can be tested experimentally.     

Brieftauben

Homing pigeons Homing pigeons are well known for their excellent homing abilities which allow them to return to their lofts from unknown releasing sites more than hundreds of kilometres away. Several orientation mechanisms – sun compass, earth's magnetic field, olfactory cues, visual cues – are known to be involved in homing performance as well as parameters such as motivation and experience. New technology give an insight in their homing behaviour and track preferences and it is shown that homing pigeons physiology and neurobiology seem to be functionally adapted to homing. Pigeons races are still common and it is shown how the pigeon breeder tries to maximize the success of his pigeons.     

Magnetoreception and its use in bird navigation

Recent advances have brought new insight into the physiological mechanisms that enable birds and other animals to use magnetic fields for orientation. Many birds seem to have two magnetodetection senses, one based on magnetite near the beak and one based on light-dependent radical-pair processes in the bird's eye(s). Among the most exciting recent results are: first, behavioural responses of birds experiencing oscillating magnetic fields. Second, the occurrence of putative magnetosensory molecules, the cryptochromes, in the eyes of migratory birds. Third, detection of a brain area that integrates specialised visual input at night in night-migratory songbirds. Fourth, a putative magnetosensory cluster of magnetite in the upper beak. These and other recent findings have important implications for magnetoreception; however, many crucial open questions remain.     

Orientation cues used by migratory birds: A review of cue-conflict experiments

During the late 1960s and early 1970s the accumulating evidence of magnetic orientation forced the conclusion that the orientation of migratory birds and homing pigeons is based upon multiple stimuli. 'Cue-conflict experiments' have provided a powerful means of asking how these directional cues relate one to another. The weight of evidence suggests that in short-term orientation decision making, magnetic cues take precedence over stars, and visual information at sunset overrides both these stimuli. Recent experiments point to polarized skylight patterns as the relevant cue in dusk orientation. Although cue-conflict experiments have now been performed on a diversity of species, generalizations are weakened because of differences in experimental design, in the cues examined and in our ability to manipulate those cues. There remains a need for carefully designed comparative studies.     

Bird navigation: what type of information does the magnetite-based receptor provide?

Previous experiments have shown that a short, strong magnetic pulse caused migratory birds to change their headings from their normal migratory direction to an easterly direction in both spring and autumn. In order to analyse the nature of this pulse effect, we subjected migratory Australian silvereyes, Zosterops lateralis, to a magnetic pulse and tested their subsequent response under different magnetic conditions. In the local geomagnetic field, the birds preferred easterly headings as before, and when the horizontal component of the magnetic field was shifted 90 degrees anticlockwise, they altered their headings accordingly northwards. In a field with the vertical component inverted, the birds reversed their headings to westwards, indicating that their directional orientation was controlled by the normal inclination compass. These findings show that although the pulse strongly affects the magnetite particles, it leaves the functional mechanism of the magnetic compass intact. Thus, magnetite-based receptors seem to mediate magnetic 'map'-information used to determine position, and when affected by a pulse, they provide birds with false positional information that causes them to change their course.     

Evidence that pigeons orient to geomagnetic intensity during homing

The influence of the Earth's magnetic field on locomotory orientation has been studied in many taxa but is best understood for homing pigeons (Columba livia). Effects of experimentally induced and naturally occurring perturbations in the geomagnetic field suggest that pigeons are sensitive to changes in geomagnetic parameters. However, whether pigeons use the Earth's magnetic field for position determination remains unknown. Here we report an apparent orientation to the intensity gradient of the geomagnetic field observed in pigeons homing from sites in and around a magnetic anomaly. From flight trajectories recorded by GPS-based tracking devices, we noted that many pigeons released at unfamiliar sites initially flew, in some cases up to several kilometres, in directions parallel and/or perpendicular to the bearing of the local intensity field. This behaviour occurred irrespective of the homeward direction and significantly more often than what was expected by random chance. Our study describes a novel behaviour which provides strong evidence that pigeons when homing detect and respond to spatial variation in the Earth's magnetic field--information of potential use for navigation.     

Avian Magnetoreception: Elaborate Iron Mineral Containing Dendrites in the Upper Beak Seem to Be a Common Feature of Birds

The magnetic field sensors enabling birds to extract orientational information from the Earth''s magnetic field have remained enigmatic. Our previously published results from homing pigeons have made us suggest that the iron containing sensory dendrites in the inner dermal lining of the upper beak are a candidate structure for such an avian magnetometer system. Here we show that similar structures occur in two species of migratory birds (garden warbler, Sylvia borin and European robin, Erithacus rubecula) and a non-migratory bird, the domestic chicken (Gallus gallus). In all these bird species, histological data have revealed dendrites of similar shape and size, all containing iron minerals within distinct subcellular compartments of nervous terminals of the median branch of the Nervus ophthalmicus. We also used microscopic X-ray absorption spectroscopy analyses to identify the involved iron minerals to be almost completely Fe III-oxides. Magnetite (Fe II/III) may also occur in these structures, but not as a major Fe constituent. Our data suggest that this complex dendritic system in the beak is a common feature of birds, and that it may form an essential sensory basis for the evolution of at least certain types of magnetic field guided behavior.     

Does pigeon homing depend on stimuli perceived during displacement?

Summary In order to test whether stimuli perceived during passive displacement are important for the subsequent homing, pigeons were transported in an apparatus designed to prevent them from receiving relevant information: The experimental birds were continuously rotated quite rapidly (1.5 cps, radial acceleration about 4 g); in addition, they were exposed to an artificial magnetic field and supplied with bottled air. Control birds were transported in open-air cages on top of the van with free view to all sides.Five pairs of releases from equal distances in opposite directions were conducted. Experienced birds were released at distances of about 15, 90, and 300 km from the loft, inexperienced birds at distances of about 180km. In each pair of releases both groups of pigeons were significantly homeward oriented. Neither in initial orientation nor in homing performance nor in the distribution of recoveries were the experimental birds inferior to the controls or in any perceptable way different from them.It is concluded that homing of passively displaced pigeons is not primarily based on information gathered during the outward journey.Abbreviations EP experimental pigeon(s) - CP control pigeon(s) The possibility to maintain our pigeon loft in a building that belongs to the Zoological Institute (Prof. M. Lindauer) of the University of Würzburg is gratefully acknowledged.     

Clustered magnetite nanocrystals cross-linked with PEI for efficient siRNA delivery

Magnetofection has been utilized as a powerful tool to enhance gene transfection efficiency via magnetic field-enforced cellular transport processes. The accelerated accumulation of nucleic acid molecules by applying an external magnetic force enables the rapid and improved transduction efficiency. In this study, we developed magnetite nanocrystal clusters (PMNCs) cross-linked with polyethylenimine (PEI) to magnetically trigger intracellular delivery of small interfering RNA (siRNA). PMNCs were produced by cross-linked assembly of catechol-functionalized branched polyethylenimine (bPEI) around magnetite nanocrystals through an oil-in-water (O/W) emulsion and solvent evaporation method. The physical properties of PMNC were characterized by TEM, DLS, TSA, and FT-IR. Finely tuned formulation of clustered magnetite nanocrystals with controlled size and shape exhibited superior saturation of magnetization value. Magnetite nanocrystal clusters could form nanosized polyelectrolyte complexes with negatively charged siRNA molecules, enabling efficient delivery of siRNA into cells upon exposure to an external magnetic field within a short time. This study introduces a new class of magnetic nanomaterials that can be utilized for magnetically driven intracellular siRNA delivery.     

Hippocampal participation in the sun compass orientation of phase-shifted homing pigeons

The orientation of phase-shifted control and hippocampal lesioned homing pigeons with previous homing experience was examined to investigate the possible participation of the hippocampal formation in sun compass orientation. Hippocampal lesioned pigeons displayed appropriate shifts in orientation indicating that such birds possess a functional sun compass that is used for orientation. However, their shift in orientation was consistently larger than in control pigeons revealing a difference in orientation never observed in pigeons that have not undergone a phase shift. Although alternative interpretations exist, the data suggest the intriguing possibility that following a change in the light-dark cycle, the hippocampal formation participates in the re-entrainment of a circadian rhythm that regulates sun compass orientation.     

Aus der Geschichte der Orientierungsforschung

Zusammenfassung Die Arbeit schildert die Entwicklungen auf dem Gebiet der Orientierungsforschung und den Wandel der Ansichten im Laufe der Zeit. Am Anfang stand Mitte des letztenJh. v. Middendorffs Vermutung, Zugvögel würden sich nach einem Magnetkompaß orientieren.Viguier diskutierte die Möglichkeit, verfrachtete Vögel würden anhand des Magnetfelds heimfinden, währendExner undReynaud kinästhetische Orientierungsmechanismen vermuteten. Erste Versuche, diese Hypothesen experimnentell zu bestätigen, blieben erfolglos.Anfang dieses Jh. versuchte man durch Verfrachtungsversuche festzustellen, unter welchen Umständen und über welche Entfernungen sich Vögel orientieren können. Seevögel zeigten sehr gute Heimkehrleistungen auch aus unbekanntem Gelände; die Versuche mit Brieftauben führten dagegen zu dem Schluß, Vögel könnten sich nur anhand bekannter Landmarken orientieren. In den 30er Jahren machten die systematischen Verfrachtungsversuche vonRüppell undWojtusiak jedoch deutlich, daß auch Stare und Schwalben von unbekannten Orten über große Entfernungen mit beachtlicher Geschwindigkeit heimkehren konnten. Die gleichzeitig begonnenen Versuche der Vogelwarte Rossitten und Helgoland zur Analyse des Vogelzugs ergaben, daß das Zugverhalten von den Bedingungen, unter denen die Vögel lebten, und bei sozialen Arten auch von Artgenossen mitbestimmt wird. Wildvögel zeigten bemerkenswerte Orientierungsleistungen, doch deren Grundlage blieb weiterhin offen.In den 40er Jahren führten die Untersuchungen vonHeinroth &Heinroth an Brieftauben abermals zu der Vermutung, die Heimkehr nach Verfrachtung beruhe auf mehr oder weniger systematischem Suchen, bis die Vögel auf bekanntes Gelände treffen; dann würden sie sich nach vertrauten Landmarken orientieren. Diese Ansicht fand weite Verbreitung;Yeagleys Hypothese einer Orientierung nach Magnetfeldparametern und der Coriolis-Kraft konnte sich nicht durchsetzen.Methodische Neuerungen leiteten Anfang der 50er Jahre die systematische experimentelle Analyse der Vögel ein.Kramer beschrieb den Sonnenkompaß und stelle mit dem Karte-Kompaß-Prinzip eine erste umfassende Theorie der Orientierung vor, die davon ausgeht, daß bei jedem Orientierungsvorgang ein externes Referenzsystem — ein Kompaß — beteiligt ist. Die Untersuchungen der Folgezeit führten zu einem recht guten Verständnis der Zugorientierung. Das Heimfinden nach Verfrachtung ist dagegen immer noch ein offenes Problem; keine der derzeit diskutierten Hypothesen kann alle bekannten Phänomene erklären. Es mehren sich jedoch die Hinweise, daß das Navigationssystem sehr variabel und in hohem Maße redundant ist, so daß mit einer einfachen Antwort gar nicht zu rechnen ist.

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On the history of orientation research

Summary This paper describes the developments and changes of ideas in the field of bird orientation research, which began in the middle of last century when v.Middendorff first suggested magnetic compass orientation in migrating birds. Still in the 19th century, two different hypotheses were proposed to explain homing.Viguier suggested that the birds made use of the spatial distribution of magnetic parameters, whereasExner andReynaud assumed that the birds were able to trace the route of the outward journey kinaesthetically. Attempts to obtain experimental support for either theory were unsuccessful.The first three decades of this century were characterized by displacement experiments designed to learn under what conditions and over what distances birds were able to return. The results obtained with seabirds indicated much more sophisticated navigational abilities than the experiments with homing pigeons, which led authors to believe that birds oriented by following familiar landmarks and could only return from unknown sites if they by chance reached a familiar region. This view became widely accepted when it was presented in the review articles ofWarner andStresemann.In the 1930s, however, systematic displacement experiments with wild birds changed the general views on orientation completely.Rüppell andWojtusiak showed that Starlings and Swallows could return from unknown sites over large distances with considerable speed. At the same time, the Vogelwarten (bird banding stations) Rossitten and Helgoland initiated programs to obtain more information on the nature of migratory orientation. The results indicated that migratory behavior can be modified by the conditions under which the birds live and, in social species, by conspecifics.Drost's experiment with Sparrowhawks gave the first indications that young birds and adult birds use different orientation mechanisms. Remarkable navigational abilities were demonstrated in wild birds, yet the mechanisms they used, were still unknown.The ideas on orientation changed again in the 1940s, whenHeinroth &Heinroth reported the resuls of their study on the orientation of homing pigeons. They suggested that pigeons, when released in an unfamiliar area, searched until they meet familiar terrain and then oriented by landmarks known from previous flights.Grifffin, whose attempts to interfer with homing by depriving displaced birds of magnetic and kinaesthetic information had failed, held similar views. A new global hypothesis byYeagley, suggesting that homing pigeons made use of a grid map formed by isolines of Coriolis force and vertical intensity of the magnetic field, was not accepted.In 1950, methodological innovations byKramer andMatthews brought new impetus to orientation research: It became possible to measure the directional tendencies of caged migrants, which allowed a systematic analysis of migratory orientation in the laboratory. At the same time, the vanishing bearings of displaced birds were found to be closely related to the home direction, which opened up new possibilities in pigeon homing.Kramer, who had described the sun compass as the first known orientation mechanism in birds, also contributed substantially to the theoretical framework of orientation by his map and compass-concept which states that an external reference system — a compass — is always involved in determining the home direction.The following period of experimental analysis began with a controversis on the role of the sun. Experimental evidence did not support sun navigation, but rather indicated that the sun was used as a compass. The analysis of the birds' orientation system during the last 30 years led to a fairly good understanding of migratory orientation. The processes of homing, however, are still not well understood. Many of the old concepts and new ones like olfactory orientation have been discussed, without any one hypothesis being able to explain all known phenomena. Recent findings suggest that there may not be one simple answer to the question of how birds navigate, as the birds' navigational system turns out to be redundant and highly variable.

     

Geomagnetic information modulates nocturnal migratory restlessness but not fueling in a long distance migratory songbird

Geomagnetic cues have been shown to influence migratory orientation and migratory fuelling in night‐migratory songbird species. Here, we used captive‐bred northern wheatears Oenanthe oenanthe from the southern Norwegian population to show that other aspects of the birds’ migratory program can be influenced by magnetic cues as well. We observed that the amount of migratory restlessness increased strongly with progression of the migratory season when the birds were kept constantly in the magnetic field of northern Germany, but the amount of migratory restlessness decreased when the magnetic field changed along the birds’ natural flyway are simulated. Thus, the Earth's magnetic field can also act as a ‘signpost’ cue for fine‐tuning the spatio‐temporal course of migration.     

Do release-site biases reflect response to the Earth's magnetic field during position determination by homing pigeons?

How homing pigeons (Columba livia) return to their loft from distant, unfamiliar sites has long been a mystery. At many release sites, untreated birds consistently vanish from view in a direction different from the home direction, a phenomenon called the release-site bias. These deviations in flight direction have been implicated in the position determination (or map) step of navigation because they may reflect local distortions in information about location that the birds obtain from the geophysical environment at the release site. Here, we performed a post hoc analysis of the relationship between vanishing bearings and local variations in magnetic intensity using previously published datasets for pigeons homing to lofts in Germany. Vanishing bearings of both experienced and naïve birds were strongly associated with magnetic intensity variations at release sites, with 90 per cent of bearings lying within ±29° of the magnetic intensity slope or contour direction. Our results (i) demonstrate that pigeons respond in an orderly manner to the local structure of the magnetic field at release sites, (ii) provide a mechanism for the occurrence of release-site biases and (iii) suggest that pigeons may derive spatial information from the magnetic field at the release site that could be used to estimate their current position relative to their loft.     

Migratory orientation of European Robins is affected by the wavelength of light as well as by a magnetic pulse

The object of this study was to test the alternative hypotheses of magnetoreception by photopigments and magnetoreception based on magnetite. Migratory European Robins, Erithacus rubecula, were tested under light of different wavelengths; after these tests, they were subjected to a brief, strong magnetic pulse designed to alter the magnetization of single domain magnetite. In control tests under white light, the birds preferred the normal, seasonally appropriate migratory direction. Under 571 nm green light, they continued to be well oriented in the migratory direction, whereas under 633 nm red light, their behaviour was not different from random. The magnetic pulse had a significant effect on migratory orientation, but the response varied between individuals: some showed a persistent directional shift, while others exhibited a change in scatter; one bird was seemingly unaffected.These findings indicate a light-dependent process and, at the same time, suggest an involvement of magnetizable material in migratory orientation. They are in agreement with the model of a light-dependent compass and a magnetite-based map, even if some questions concerning the effect of the pulse remain open.