Experimental studies of the development of migratory orientation mechanisms

Summary Recent experimental studies (since ca 1985) on the ontogeny of orientation mechanisms in migratory birds are reviewed. The processes and interactions are synthesized into a framework that may help identify critical research questions. Birds that grow up in the earth's magnetic field develop the ability to perform appropriate migratory orientation even in the absence of any experience with relevant visual cues. In two species, large changes in direction during the course of migration seem to be controlled by an endogenous time program. In one of these, the pied flycatcher (Ficedula hypoleuca), the correct magnetic orientation seems to occur only when the magnetic fields appropriate to the latitudes encountered en route were experienced at the proper seasonal time. The magnetic compass may be modified by visual experience with either the daytime or night sky. Celestial rotation may be the calibrating reference in this case, as it is in the development of the star compass. Young Savannah sparrows (Passerculus sandwichensis) learn to perform compass orientation at sunset based on polarized skylight. This compass capability seems to be calibrated by magnetic directions. Some problems of experimental design and the interpretation of results from experiments on development are discussed.     

Magnetic inclination compass: A basis for the migratory orientation of birds in the Northern and Southern Hemisphere

We conducted orientation experiments with Silvereyes,Zosterops lateralis, Australian passerine migrants, to see whether birds living in the Southern Hemisphere in a magnetic field with an upward inclination orient in the same way as birds in the Northern Hemisphere that experience a downward inclination of the magnetic field. Tested indoors in the local geomagnetic field, the birds preferred southerly directions corresponding to their migratory direction in spring. In a magnetic field with a reversed vertical component, they reversed their directional tendencies. This shows that the magnetic compass of Silvereyes also functions as an inclination compass based on the inclination of the field lines instead of the polarity.     

Ecological causes and consequences of bird orientation

Summary An advanced orientation capability offers possibilities for birds to optimize movement patterns in a wide variety of ecological situations. The adaptive significance of different patterns of angular dispersion and of orientation responses to topography and sociality are elucidated. The orientation capacity is characterized by flexibility, exemplified by reorientation promoting safety and restoration of fat reserves during migration. There are also limitations to the orientation process, leading to costs of migration through mis- or disorientation, and to constraints on the evolution of routes and timing of migratory flights. Young migrants may acquire an erroneous compass sense, and misorient several thousands of kilometers off their normal course. Widespread and dense fog of long duration causes disorientation and mortality among land birds migrating over the sea. Orientational constraints in the evolution of migration routes may be most easily disclosed at high geographic and magnetic latitudes. Here the birds are faced with special difficulties in using their celestial as well as their magnetic compasses. The sun compass could be used for great circle orientation, but observed spring flight trajectories of high arctic shorebirds and geese seem to conform with rhumbline routes.     

A magnetic pulse leads to a temporary deflection in the orientation of migratory birds

Migratory Australian Silvereyes were treated with a strong magnetic pulse designed to alter the magnetization of the small magnetite particles that are found in birds' heads. Prior to the treatment, the birds preferred the northeasterly migratory direction. The pulse initially resulted in a 90° clockwise shift of orientation; however, within about a week, the birds seemed to return to their original headings. These findings, which seem to suggest an involvement of magnetite in migratory orientation, are in contrast with previous findings which indicated that it is a light-dependent process. They are discussed in view of the current concepts on magnetoreception and on the role of magnetic information in avian orientation.     

Spatiotemporal programs and genetics of orientation

Summary A number of migratory bird species have endogenous annual rhythms that regulate the entire annual cycle including the migratory portion. Moreover, captive migrants display inherited migratory activity; this could theoretically also be used by free-living migrants as a time-program for migration. Finally, this heritable migratory activity is oriented in a seasonally appropriate direction even in naive birds. These, characteristics should enable inexperienced migrants isolated from contact with experienced conspecifics to utilize a heritable vector-navigation program to migrate from the breeding grounds to the winter quarters. That is, migrants should reach goal areas they have never experienced by migrating in programmed directions, for as long a period as the genetically fixed time-program for migratory activity induces them to do so. The time-course of migration as established by trapping stations, theoretical influences of environmental variables on migratory programs, and also compensatory behavior and migratory backup measures, are discussed. The present evidence supports the view that a large number of migrants are essentially brought to their wintering areas by vector-navigation systems.     

Conceptual approaches to avian navigation systems

Summary The general basis of migratory orientation in birds is most probably an endogenous time-and-direction program. Directions are selected with respect to celestial and geomagnetic clues. Using these clues, a bird may reach a large population-specific area; however, it will hardly be able to find a particular location, for instance its previous breeding site. Homing to a familiar site over several hundred kilometres of unfamiliar terrain appears to be based on the smelling of atmospheric trace compounds. Conceptual approaches to the mechanism of olfactory navigation have as yet only reached an early state of speculation.     

Sensory basis of bird orientation

Summary Sensory information which may be essential for the complex process of orientation of birds is described in this article. The use of vibrational, visual, chemical, olfactory, magnetic cues and their receptive mechanisms, as far as they are known, are explained. Special reference is given to the behavioral and physiological aspects of magnetic sensitivity.     

Sensory basis of bird orientation

Sensory information which may be essential for the complex process of orientation of birds is described in this article. The use of vibrational, visual, chemical, olfactory, magnetic cues and their receptive mechanisms, as far as they are known, are explained. Special reference is given to the behavioral and physiological aspects of magnetic sensitivity.     

Depolarization of natural skylight disrupts orientation of an avian nocturnal migrant

Summary Given a view of clear evening skies, migratory blackcaps (Aves:Sylvia atricapilla) orient appropriately in the absence of meaningful information from the geomagnetic field. When the intensity of natural skylight polarization patterns was reduced with pseudodepolarizers by over 90%, test birds were disoriented, and their migratory restlessness in autumn was drastically reduced.     

Magnetic compass orientation in the subterranean rodentCryptomys hottentotus (Bathyergidae)

Summary To test whether mole-ratsCryptomys hottentotus were able to use the magnetic field for orientation, laboratory experiments were conducted which were based on the animals' spontaneous tendency to build their nests at the same position in a circular arena. In the local geomagnetic field, the animals preferred the SE-sector. When magnetic north was turned by 120^o or by 180^o, the mole-rats changed their nest position accordingly. This clearly shows that they can use the magnetic field for direction finding.     

Recent advances in cerebellar granule cell migration

In the developing brain, postmitotic neurons exhibit dynamic changes in mode, direction, tempo and rate of migration as they traverse different cortical layers. Such changes in cell migration require orchestrated activities of multiple guidance cues and transmembrane signals. In this article, we first describe when, where and how cerebellar granule cells alter their migratory behavior during the entire course of their migration. We then present how internal (inherent) programs regulate the sequential changes in the migratory behavior of granule cells in vitro. Finally, we discuss the roles of external guidance cues and transmembrane signals in controlling granule cell migration.     

Overcast tests with clock-shifted pigeons

In order to investigate the pigeon's compass mechanism, a series of overcast tests with clock-shifted birds were run at two familiar release sites. While controls were able to assume a correct homeward direction, the experimental birds' initial orientation cannot be explained either on the basis of a time-compensated sun compass or of a time-independent magnetic compass. Speculative explanations of our paradoxical results are attempted.     

The sun compass

Summary The sun compass was discovered by G. Kramer in caged birds showing migratory restlessness. Subsequent experiments with caged brids employing directional training and clock shifts, carried out by Hoffmann and by Schmidt-Koenig, showed that sun azimuth is used and sun altitude ignored. McDonald found the accuracy to be ±3^o–±5^o. According to Hoffmann and to Schmidt-Koenig, caged birds trained at medium northern latitudes were able to allow for the sun's apparent movement north of the arctic circle but not in equatorial and trans-equatorial latitudes.In homing experiments, and employing clock shifts, Schmidt-Koenig demonstrated that the sun compass is used by homing pigeons during initial orientation. This finding supports the existence of a map and compass navigational system. Pigeons living in equatorial latitudes utilize the sun compass even under the extreme solar conditions of equinox (Ranvaud, Schmidt-Koenig, Ganzhorn et al.). The use of the sun compass during zenith passage of the sun is being investigated.     

Evolutionary aspects of orientation and migration in birds

Summary Evolutionary aspects of avian migratory orientation and navigation are reviewed. A theoretical approach to the evolution of complex (endogenously programmed) migratory behavior is presented using the comparative method of ordering a progression in existing behavioral characteristics from dispersal, to facultative migration, to obligate migration.     

Concept of an extracellular regulation of muscular metabolic rate during heavy exercise in humans by psychophysiological feedback

Efferent motor signals to skeletal muscles concern not only the space/time pattern of motion, but also the setting of muscular performance and through this the control of the current metabolic rate. For an optimal adjustment of metabolic rate during heavy exercise — e.g. in athletic competitions — a feedback control system must exist, including a programmer that takes into consideration a finishing point (teleoanticipation). The presented experiments, using Borg's scale, indicate the existence and functioning of a system for optimal adjustment of performance during heavy exercise and the relevance of teleoanticipatory effects. Thus motor learning includes not only somatosensory control, but also metabolic control. With regard to migratory birds, such metabolic control would have to operate in the individual as well as in the migrating flock as a whole.     

Metabolism-weight relationship in some small nonpasserine birds

Summary The metabolism — weight relationship 24 different nonpasserine birds follows the equation M=0.138 W^0.716. No pronounced differences could be found, relating to the metabolic rate per unit body weight, between these birds and representatives of the order Passeriformes.     

Some observations on the Rohon-Beard cell perikaryon

Summary During the hatching period, the Rohon-Beard cells of Salmo gairdneri showed definite structural maturity of their perikarya, which is in contrast to the amphibian species investigated, where neuronal maturation of the Rohon-Beard cells is finished only in later — posthatching — developmental stages.     

Exploring oligodendrocyte guidance: ‘to boldly go where no cell has gone before’

Oligodendrocytes, the myelinating cells of the central nervous system (CNS), originate early in the formation of the brain in specific foci, and migrate throughout the parenchyma. The instructional cues guiding the migration of these progenitor cells must be encoded into their developing environment. Soluble factors as well as membrane-bound cues most likely synergize to create a complex thoroughfare needed to sculpt and organize the brain into a functional organ with white and gray matter. Classically, the focus of many guidance related studies in the CNS has been limited to neuron physiology. However, It is becoming increasingly clear that their lifelong partners, oligodendrocytes, express both ligands and receptors able to both present and respond to these classical cues. In this short review, some recent findings in the Semaphorin and Eph fields will be presented with respect to oligodendrocyte expression and function.Received 4 November 2004; received after revision 1 December 2004; accepted 7 December 2004     

Migratory patterns of clonally related cells in the developing central nervous system

Summary Neurons and glioblasts that arise in the ventricular zone migrate to form discrete nuclei and laminae as the central nervous system develops. By stably labeling precursor cells in the ventricular zone, pathways taken by different cells within an individual clone can be described. We have used recombinant retroviruses to label precursor cells with a heritable marker, theE. coli lacZ gene; clones of lacZ-positive cells are later mapped histochemically. Here we review results from three regions of the chicken central nervous system — the optic tectum, spinal cord, and forebrain - and compare them with previous results from mammalian cortex and other regions of the vertebrate CNS. In particular, we consider the relationship between migratory patterns and functional organization, the existence of multiple cellular sources of migratory guidance, and the issue of whether a cell's choice of migratory pathway influences its ultimate phenotype.     

Getting there and being there in the cerebral cortex

The mammalian neocortex is composed of functional areas that are specified to process particular aspects of information. How is this specification achieved during development? Since cells migrate to their final positions in the developing nervous system, a central issue is the relation between cellular migration and positional information. This review combines evidence for early positional specification in the developing cortex with evidence for cellular dispersion during migration. A model is suggested whereby stable cues provide positional information and minorities of ‘displaced’ cells are respecified accordingly. Comparison with other parts of the CNS reveals that cellular dispersal is ubiquitous and has to be included in any mechanism relaying positional specification. Ontogenetic and phylogenetic considerations suggest that radial glial cells might provide the positional information in the developing nervous system.