Bird orientation and the geomagnetic field: A review

Neuroscience & Biobehavioral Reviews, Vol. 2, pp. 255-270. Printed in the U.S.A.

Bird Orientation and the Geomagnetic Field: A Review KLAUS-PETER OSSENKOPP AND RAPHAEL BARBEITO 1

D e p a r t m e n t o f Psychology, York University, Downsview, Canada ( R e c e i v e d 24 M a y 1978) OSSENKOPP, K.-P. AND R. BARBEITO. Bird orientation and the geomagnetic field: A review. NEUROSCI. BIOBEHAV. REV. 2(4) 255-270, 1978.--The possibility that birds use the geomagnetic field to guide their orientation has been repeatedly suggested over the last century. Early attempts to experimentally verify this hypothesis were largely unsuccessful. Recently, however, this issue has been more thoroughly examined, from a variety of approaches, with positive results. Magnetic fields have been shown to have a biological effect on a variety of animals ranging from unicellular organisms to mammals. Many of these organisms, including birds, show changes in orientation behavior as a result of changes in the ambient magnetic field. Specific data supporting the existence of a "magnetic-compass" in birds include demonstrations that (a) changes in the intensity of the ambient magnetic field disrupt various kinds of orientation behavior and (b) that systematic changes in the direction of the ambient magnetic field are accompanied by systematic changes in the direction of orientation. The biggest obstacle in further study of the "magnetic-compass" is the almost complete ignorance of the biophysical mechanism(s) involved in the biological detection of the geomagnetic field. Some theoretical speculations about possible biomagnetic mechanisms are discussed and suggestions for the direction of future research on the "magnetic-compass" and its relation to other orientation behaviors are provided. Bird orientation

Geomagnetic field

Biomagnetic effects

IT WAS early recognized by Kramer [72] that in order for any animal to find its way home in strange territory, it must possess two abilities: it must know the direction of the home site, i.e., have some sort of " m a p , " and it must have some way of telling direction, i.e., possess a " c o m p a s s . " Most of the recent research on orientation has concentrated on determining the mechanism(s) underlying the "compass" component of this ability; the " m a p " component usually remaining at the level of a hypothetical construct. The following review will concern itself with the issue of the geomagnetic field as a source of information for the "compass" mechanism used in bird orientation. The purposes of this review are first to give an overview of the research literature in a manner which facilitates an assessment of the fruitfulness of each of the various methodological approaches used in this area, and second to delineate some of the problems associated with this research area in general. Two previous reviews on bird orientation [47,65], although critically examining individual studies related to bird orientation and the geomagnetic field, have not presented a clear oganization of the literature along methodological lines and have not addressed themselves to the general problems dealt with in the present review. Thus, this review provides a quite different perspective from the two previous reviews in this research area. Additionally, this paper will deal with suggested mechanisms for the "magnetic-

compass," as well as including the literature published since these earlier reviews.

Some Characteristics of the Geomagnetic Field The earth acts like a great spherical magnet in that it is surrounded by a magnetic field. The measurement of the geomagnetic field at any place on its surface consists of determining the direction and intensity of that field. This can be accomplished by obtaining information on three parameters: the magnetic declination, inclination, and field intensity. The magnetic declination is a measure of the difference between the true meridian, i.e., a circle through the geographical poles and the N-S direction shown by a compass--the magnetic meridian. The inclination or dip is the angle which the lines of force of the geomagnetic field make with the plane of the horizon. And one measure of the intensity of the field is the horizontal intensity. These three parameters give a complete vector representation of the total field. The earth contains magnetic poles (not identical with the geographic poles) defined by the points at which the dip is 90° and horizontal intensity is zero. The magnetic equator is an imaginary line at which the dip is 0°. The magnetic field surrounding the earth is very irregular so observations must be made in many places on the surface in order to get a satisfactory picture of these variations. Local anomalies,

1The preparation of this paper was supported by a National Research Council of Canada grant to Dr. N. I. Wiener (No. AP301) and by National Research Council of Canada Postgraduate Scholarships to the authors. We would like to thank Drs. I. P, Howard, M. A. Persinger and N. I. Wiener for critical reading of an earlier version of this manuscript, and P. R. Sanberg for his valuable suggestions. The financial assistance of the York University Psychology Graduate Student Assoc. is also appreciated. Please send all reprint requests to the first author, Department of Psychology, University of Western Ontario, London, Ontario N6A 5C2, Canada.

C o p y r i g h t © 1978 A N K H O I n t e r n a t i o n a l Inc.--0149-7634/78/040255-16502.10/0

256

O S S E N K O P P AND BARBEITO

due to geological formations containing magnetic material, or resulting from man made sources, distort the geomagnetic field in those localities. However, since the effect of magnetic material decreases rapidly with increasing distance, magnetic anomalies are attenuated with altitude. Transient variation in the earth's magnetic field occurs as a result of a number of terrestrial and non-terrestrial causes. There are slight solar and lunar daily variations in the field and from time to time a variety of more intense fluctuations called magnetic storms occur. Any marked degree of natural disturbance is classed as a magnetic storm. One measure of the intensity of magnetic disturbance that has proven very useful is the three-hour range K-index. F o r this measure, a figure ranging from 0 to 9 is assigned for each interval of 3 hr with each number representing a specific range of magnitude of disturbance for the most disturbed element (usually hori~ zontal intensity) during the 3 hr interval. The intensity of the disturbance is measured in gammas (1 g a m m a = l0 "~oersted or Oe). The earth's field itself has very roughly a value of about 0 . 5 0 e such that a K-index of 7, which has a lower limit of about 200 gamma, represents a change of about 0.4% in field intensity. A K-index of 5 represents moderate disturbance, 8 or 9 indicates severe magnetic storm activity. (For a more complete description of the geomagnetic field, see

[98]). THE EXPERIMENTAL STUDIES

Criteria for Establishing the Existence of a "MagneticCompass" To establish the existence of a "magnetic-compass" two criteria must be met. First, it is necessary to establish that birds can indeed detect the geomagnetic field, and second, it is necessary to demonstrate that the bird is responding to information from the geomagnetic field by showing appropriate orientation behavior. The experimental evidence dealing with these criteria follow in the next several sections.

Biomagnetic Effects in Non-avian Species Compelling support for a biological effect of magnetic fields can be recruited from studies on organisms other than birds. A number of studies have demonstrated that magnetic fields can have a biological effect on primitive unicellular and multicellular organisms [17, 103, 104, 145], planarians and mollusks [8, 24, 25, 26, 27, 30, 31, 33,116], insects of various kinds [11, 12, 13, 14, 16, 80, 81,111,125, 126, 127, 146, 154], fish [3, 4, 15, 21, 89, 90, 122, 155], salamanders [110] and even mammals [51, 96, 97, 109, 113,138]. Although some of these studies involved atypical magnetic fields, i.e., fields that were fluctuating rather than static or fields of abnormally high intensity, most involved static fields which were often near natural intensity levels (e.g., F. A. Brown's monumental work on planaria and snails). Of special interest are the experiments demonstrating magnetic field induced changes in some type of orientation behavior in non-avian species. Blakemore [17] demonstrated a magnetotactic response in bacteria (Spirochaeta plicatilis). Palmer [104] found he could alter the spatial orientation of a green alga (Volvox aureus) by applying a 5 0 e magnetic field at a right angle to the earth's field. In a controversial series of studies, Brown and his coworkers showed that the compass-directional orientation of the mudsnail (Nassarius obsoletus) could be altered by applying low intensity (0.171.50 Oe) magnetic fields to these animals [22, 28, 29, 32, 34].

Planarian worms (Dugesia dorotocephala) revealed a comparable compass-directional phenomenon that could be influenced by applied magnetic fields [23, 25, 30]. Becket [12] and Becker and Speck [16] showed that various species of flies preferred certain orientations with respect to the geomagnetic or to imposed magnetic fields, when landing and in a resting position on an illuminated surface. A similar response was found in Drosophila melanogastor [!11], in termites (Odontotermes latericius and Macroterrnes bellicosus) [11] and in Melontha [126,127]. Becker [14] also found that magnetic fields could influence the direction in which termites (Coptotermes arnanii and Heterotermes indicola) built their tunnels connecting the nest and various food sources. In an excellent study on honeybees (Apis mellifera, Apis meUifica) [81, 82, 85], it was demonstrated that the honeybees' waggle dance on a vertical comb is influenced by the earth's magnetic field and by artificial fields. Finally, a demonstration that resting or inactive goldfish (Carassius auratus) prefer certain orientations with respect to the geomagnetic field was provided by Becker [15]. Phillips [ 110] trained salamanders (Eurycea lucifuga) to move down a runway to a moist limestone-filled compartment. Magnetic cues, provided by the direction of a magnetic field (0.47 Oe) with respect to the runway, indicated which end of the runway contained the moist goalbox. The salamanders were able to move to the correct compartment on the basis of the magnetic cues provided, thus indicating that these animals may use the earth's magnetic field as a source of directional information. These studies not only demonstrate that a biomagnetic effect can be found in a variety of animal species but they also demonstrate that the orientation behavior of organisms other than birds can be altered by imposed magnetic fields (see also review by Martin and Lindauer [841).

Biological Effects of Magnetic Fields The problem of demonstrating that birds can detect the geomagnetic field can be approached in two ways. One might attempt to demonstrate that exposure to a magnetic field (other than the earth's) can produce some physiological or behavioral changes in a species of bird. While this type of result would establish that exposure to a magnetic field can have some biological consequences it would not be evidence that the bird is able to " d e t e c t " the field and thus gain some kind of information from it. To demonstrate detection of the field, the bird's behavior must be brought under the stimulus control of a magnetic cue (cf. [92]). The stimulus control studies will be discussed in a later section.

Biobehavioral consequences of exposure to magnetic fields. There are some data which indicate that the exposure to a magnetic field other than the earth's can affect birds in a way not directly related to orientation. Increased motor activity was found in five species of birds exposed to a constant, relatively homogeneous field of 0 . 6 - 1 . 7 0 e [45]. Increased ambulation and defecation of Peking ducklings (Anas platyrhynchos) in an open field test was found to be related to the intensity of the magnetic field during prenatal exposure [102] and it was found that the circadian rhythm of the house sparrow (Passer domesticus) could be entrained to a cyclic change in the intensity of the vertical component of a magnetic field [18]. Other effects have been reported which are physiological in nature. However, these studies used magnetic field strengths of abnormally high intensity, therefore it is difficult

G E O M A G N E T I S M A N D BIRD O R I E N T A T I O N to interpret the results. Yakovleva and Medvedava [170] found oedemas of the nervous tissue in the brains of adult pigeons exposed to an approximately 520 Oe magnetic field. And, Knutson [69] found an increase in the somite number in quail embryos exposed to a high intensity 1500-7000 Oe field. Effects of electromagnetic waves. Some data that has often been cited as evidence for an effect of magnetic fields on birds result from observations indicating that high intensity, high-frequency electromagnetic waves, e.g., radar beams, apparently affect the behavior of flying birds. Since electromagnetic waves have a magnetic component, the argument is that exposure to such waves with some resultant effect, could be caused by the magnetic component of the waves. Some early reports suggested the homing of pigeons and migration of wild birds were affected by radio stations [5, 36, 37, 41, 88] and radar transmitters [61, 68, 112]. While most of these observations were anecdotal, experimental verification for these observations was provided by Hochbaum [61] who reported that the flight pattern of 12 of 14 flocks of migrating ducks was disrupted when a radar beam was directed at the flock. Also important is Hochbaum's observation that flocks of blackbirds, tree swallows, Franklin's gulls, juncos and flickers were not affected by the radar beam [61]. This finding suggests that a species difference in sensitivity may account for several failures to observe any disrupting effects of radar [44, 71, 86]; a suggestion supported by Dorst's finding [43] of an interspecific variation in the response to radar. In addition to these data, studies that used low-frequency, low-intensity electromagnetic fields (for reviews of the biological effects of E L F magnetic fields see [83, 106, 108]) have also demonstrated an effect on the flight pattern of free-flying nocturnal migrants [77] and on the orientation of Ring-billed gulls (Larus delawarensis) tested in the Southern orientation apparatus [136]. Although the observations of the effects of electromagnetic waves on flying birds have been used as support for an effect of magnetic fields on birds, it must be noted these fields are pulsed or fluctuating and are not constant fields. It is doubtful that a generalization from these effects to the effects of the geomagnetic field on birds is valid. (For a possible explanation of the disrupting radar effects see [1431).

Disrupting Effects of Applied Magnetic Fields Bar magnet studies. The oldest approach in attempts to demonstrate an effect of magnetic fields on bird orientation, involves placing magnets either on the wings, body or head of the birds, and determining if the fields produced by the applied magnets cause the birds to become disoriented. Casamajor [37] was the first to try this approach and obtained negative results, as did Wodzicki et al. [168]. Yeagley's classic experiments [171] showing positive results, have been largely discounted [43, 58, 59] and subsequent experiments [19, 54, 55, 56, 87, 121, 168, 169] also failed to find any disruptive effects of attached magnets. Keeton, in several recent experiments, however, has established the usefulness of this approach [63,64]. His procedure consisted of gluing bar magnets or brass bars to the backs of pigeons. Keeton finds that birds wearing the magnets show a decrement in some aspect of homing behavior (for a review of K e e t o n ' s work prior to 1974, see [65]). Additional experimental evidence that magnets can inter-

257 fere with orientation is provided by experiments which used fledgeling Ring-billed gulls [134,135] and Herring gull (Larus argentatus) chicks [94]. Southern's technique involved cementing small ceramic magnets to the mid-dorsal surface of the heads of the experimental birds and nylon discs of comparable size, shape and weight to the heads of the control birds. The effect of the magnets was evidenced by random dispersal of the experimental birds during the orientation test. In an attempt to extend Southern's findings, Moore [94] used 3-10 day old Herring gull chicks. Using the same procedure as Southern, Moore was not able to demonstrate random orientation in the birds wearing the magnets. Instead, he found a difference in the mean directional preference between the experimental and control birds. In addition, the experimental group showed greater variance in direction chosen. Moore concluded that magnetic stimuli alter but do not completely disrupt Herring gull chick orientation. A rather novel approach to applying a disrupting magnetic field to the birds body was developed by Walcott [148,150]. He equipped pigeons with a pair of small coils and a battery. The two coils, one glued to the top of the h e a d - - t h e other serving as a collar around the neck, acted like two small Helmholtz coils when connected to the battery. Walcott was able to produce a field of 0 . 1 0 e between the coils in this manner. Control birds carried the same apparatus but with the battery not connected. Control birds carried the same apparatus but with the battery not connected. When this procedure was tested [148,150], it was observed that in 14 of 19 releases, the experimental birds were less well oriented than controls. This procedure has been used by Walcott [152] to provide more interesting data. This latter study will be discussed in a later section. There are recent studies which did not report a disruptive effect of magnets. Lamotte's [76] negative results can be discounted on methodological grounds. He fixed magnets or brass bars to the pigeons' right wings. (The magnets had a reported pole intensity of 0.38 Oe.) Unfortunately, this arrangement produces a fluctuating rather than a static field around the birds' body during flight and invalidates any direct comparison of results since different magnetic field characteristics were present. F o r an additional critical discussion of Lamotte [76], see [67]. In a different type of bar magnet magnet application, Rabol [ll5] placed bar magnets on the underside of an Emlen-funnel type apparatus [48] and tested the effects of an increased ambient magnetic field (approximately 2 - 2 . 5 0 e ) on the direction of migratory restlessness in several bird species. No disruption in the direction of orientation subsequent to the experimental manipulation could be demonstrated in Redstarts (Phoenicurus phoenicurus), Blackcaps (Sylvia atricapilla), European robins (Erithacus rubecula) and Garden warblers (Sylvia borin), under overcast sky conditions. Rabol suggests that these birds were using cues, other than stellar or magnetic in origin, for orientation. While it is difficult to interpret the meaning of Rabol's data, there is sufficient data available to conclude that magnets do affect orientation in some species of birds. Helmholtz coil produced fields and related studies. The second major approach used in attempting to disrupt orientation behavior in birds via magnetic fields involves placing the organism within an artificially created field. The simplest method is to place the bird and the test apparatus between two large Helmholtz coils or within a set of Rubens coils [123]; these arrangements produce a relatively homogeneous magnetic field. Fromme [52] placed a Kramer-cage between

258 two large Helmholtz coils. The Kramer-cage has eight radial perches and the activity on each perch is recorded. Many small birds display a behavior called migratory restlessness or "Zugunruhe". This behavior is characterized by motor responses, in the direction of normal migration, that occur during the periods of intense activity that coincide with the time of migration [70]. The Helmholtz coils within which Fromme placed the Kramer-cage, changed the direction of the resultant field by 90 ° from normal and allowed a variation in field intensity. No effect of the magnetic cues could be ascertained in tests on European robins or on Whitethroats

(Sylvia communis). In contrast, Wiltschko [156] was able to demonstrate random orientation under certain magnetic field conditions. He placed a Kramer-cage between four Helmholtz coils which allowed changing the resultant horizontal component's declination and also changed the inclination. At the same time the field intensity was varied by screening off parts of the geomagnetic field by a steel vault or increasing intensity via the coils. Field values ranged between 0.30 and 0.95 Oe; the normal geomagnetic field having a value of 0.41 Oe. When European robins were tested during spring and fall migration, Wiltschko found that under normal geomagnetic field conditions, these birds oriented appropriately without the aid of any visual cues. However, if the total intensity of the ambient magnetic field was altered via the steel vault and the Helmholtz coils (i.e., lowered to 0.30 Oe or increased to 0.75 and 0.95 Oe) random orientation behavior resulted. Further tests established that slight deviations in intensity (0.38 to 0.47 Oe) did not affect orientation. Since 0.38 Oe still produced orientation whereas 0.30 Oe did not, this suggests that these birds were differentially affected by field intensities differing by only 0.08 Oe. Subsequent tests [157] showed similar results; when the magnetic field intensity was increased or decreased beyond certain limits, random orientation occurred--within these limits, normal orientation was displayed. These findings are consistent with data obtained from some invertebrates [27]. When Whitethroats were used as the test species [162], it was found that these birds also oriented in a random fashion when the ambient field intensity was reduced from 0.46 to 0.34 Oe. Further tests on a related species, the Garden warbier, showed similar results. In addition, when the inclination of the ambient field was changed to 0°, random orientation was obtained under normal intensities [159]. Both species of Sylvia show normal orientation with a natural magnetic field condition and without the aid of visual cues. Southern [135] used a set of Rubens coils to allow adjustment in intensity, declination and inclination of the ambient fields in his test apparatus. He used a Southern-type orientation cage and his birds were Ring-billed gull chicks. Although Southern was able to obtain a random distribution in orientation behavior when the ambient field intensity was set at 0.3 Oe or at 1.2 Oe, be was unable to show reliable orientation under a normal geomagnetic field level (0.6 Oe) in his test apparatus. Thus Southern's data [135] are not interpretable. Due to low light levels necessitated by the experimental procedure, only a small percentage of the birds were displaying orientation behavior and this may have decreased the sensitivity of his tests.

Effects of Artificial Disruption and Natural Perturbances in the Geomagnetic Field Shielding studies. In conducting experiments on Euro-

O S S E N K O P P AND BARBEITO pean robins and Whitethroats, Fromme [52] obsrved that using the Kramer-cage technique, his birds showed appropriate directions in migratory restlessness under outdoor and indoor (no visual cues) conditions. However, if the Kramercage was placed inside a steel vault (which presumably alters the ambient magnetic field conditions), random orientation was obtained. Although subsequent tests with imposed magnetic fields proved inconclusive, these findings prompted Wiltschko [156] to reinvestigate the phenomenon. Wiltschko was again able to show that European robins could orient appropriately in a Kramer-cage when visual directional cues were eliminated except when the test apparatus was placed in a steel chamber. The steel chamber used by Wiltschko, reduced the ambient magnetic field intensity from 0.41 to 0.14 Oe. Under the reduced field intensity conditions the birds displayed random orientation. In contrast, placing the Kramer-cage inside a Faraday-cage (which shields out radio frequency electromagnetic waves but not E L F waves) had no effect on the normal orientation behavior. A similar demonstration was given using whitethroats [162]. A magnetically-shielded room was used by Southern [135] to reduce the ambient magnetic field from the normal intensity of 0 . 6 0 e to 0.02 Oe. A similar room but without the magnetic shielding, served as the control situation. Owing to the nature of the experimental equipment, illumination levels in both test rooms were rather low and resulted in a large percentage of the birds not displaying orientation responses. Southern found that in those animals responding, no significant directional preference could be demonstrated in either the experimental or control conditions. Thus these experiments proved inconclusive. Magnetic anomoly studies. One method of more directly testing the effects of a distorted magnetic field on orientation is to take advantage of local magnetic anomolies. In some preliminary work, Graue [57] reported that when homing pigeons were released at magnetically disturbed and undisturbed locations, the degree of scatter in the vanishing bearings appeared to be related to the amount of disturbance in the magnetic contours. When the actual flight paths of homing pigeons were compared to aeromagnetic data, a tendency was found for homing paths to skirt around or head between magnetic anomolies and to avoid steep " g r a d e s " of magnetic intensity [139, 140, 141]. Other studies found that pigeons released in an area containing a magnetic anomaly vanished in a direction to the left of the home direction and approximately in the direction of the "magnetic gradient" present [148]. Further experiments found that experienced birds were not disturbed by the anomaly, even under overcast conditions whereas, inexperienced pigeons were affected under all conditions [50]. It is rather unfortunate that this approach has not been used by more investigators, since these reports suggest that it is a promising method of investigation. Effects of fluctuations in the geomagnetic field. Another method now used by researchers in studying the effects of a disturbed geomagnetic field, involves taking advantage of the occurrence of magnetic storms. Although there had been some earlier scattered reports that suggested a deterioration of homing in pigeons during magnetic storms, Southern [ 131, 132, 133] was probably the first to present systematic data on the effects of magnetic storms (intensity of which was measured by K-index values) on orientation (reviewed in [65]). Using Ring-billed gull chicks and testing them in the Southern-type orientation apparatus, Southern was able to demonstrate that with increasing geomagnetic disturbance.

G E O M A G N E T I S M AND BIRD ORIENTATION an increase in the scatter of the response headings in his birds occurred. Thus at low K-index values, the animals selected an appropriate direction; at higher K-index values, orientation became random. More evidence that magnetic storms can influence orientation was given in a study by Keeton, Larkin and Windsor [67]. In these experiments pigeons were released over a period of time, and subsequently a correlation between the mean vanishing bearing for each test release and the K-index value at the time of the release, was calculated. The results indicated a systematic shift in bearing with an increase in the K-index value. Specifically, the bearings were more to the left (as seen by a person facing homeward at the release site) when the K-index value was high. The most conclusive evidence that natural geomagnetic disturbances are associated with disruption of orientation in birds was provided by Moore [95]. He was the first to demonstrate such an association in free-flying passerine migrants. Using both the ceilometer and the moon watch techniques, nocturnal migrants were observed during a Fall and Spring movement. The main data base, taken from the ceilometer watches, showed a statistically significant correlation which indicated that as the magnitude of geomagnetic disturbance increased the magnitude of variability in orientation increased. The data from the moon watches revealed the same relationship, as did the data from each of the migratory movements separately. Since the data presented to illustrate a relationship between magnetic storms and avian orientation behavior is correlational in nature, one cannot infer that the magnetic fluctuations caused the observed effects on orientation. However, more conclusive evidence for a causal relationship was provided in a recent study [78]. The vanishing bearing of homing pigeons, when wearing either magnets or brass bars, was correlated with K~2 values (K values summed over a 12 hr period). When the birds wore brass bars the expected disruption in orientation occurred, i.e., deviation from the homeward bearing was found to be correlated with K. However, when the birds wore magnets no correlation was found; the magnets masked the effects of a geomagnetic disturbance. Since the masking occurred when the birds, in effect, wore their own magnetic fields, whatever caused the correlation when the birds wore the brass bars was presumably magnetic in nature. Thus, Larkin and Keeton [78] have presented a strong case for a causal relationship between geomagnetic disturbances and orientation behavior in birds. While these reports show that natural geomagnetic disturbances affect various aspects of orientation behavior, other studies have met with negative results. Able [1] did not find a correlation between magnetic field activity levels and orientation in nocturnal migrants. Richardson [119,120], who used radar surveillance to monitor migrants over Puerto Rico, found that the direction of individual birds did not correlate with K-index values [119], and that while he found a significant positive correlation between magnetic disturbance and counter-clockwise heading (an effect reported in [94,95]), he did not find a relationship between the accuracy or the precision of orientation and K-index values [120]. Furthermore, Richardson [120] noted that the significant relationship he reported may have been spurious given the large number of correlations performed on his data and given that there was no other indication that such a relationship existed. In summary, the evidence on the possibility of a disruption of bird orientation by means of applied magnetic fields

259 or by disturbances in the normal geomagnetic field, seems to favour a positive effect. Although certain discrepancies in the data exist, disruption has been demonstrated in both free-flying bird orientation behavior and in the behavior of non free-flying birds.

Using Magnetic Cues to Achieve Stimulus Control Research that attempts to achieve stimulus control with magnetic cues follows the premise that the use of geomagnetic field information to ascertain direction presupposes detection. A second premise upon which this research seems to be based is the notion that any behavioral response of an organism can be conditioned to any stimulus. These two premises lead to a difficulty when interpreting negative results in studies of this nature. A failure to achieve stimulus control may be the result of the organism not being able to detect (and therefore use) the geomagnetic cue(s), or the criterion response may not be conditionable to a magnetic stimulus. Conditioning studies. Experiments that have attempted to demonstrate that some response in a bird can be brought under the stimulus control of magnetic stimuli by using conditioning procedures, have largely produced equivocal results. Orgel and Smith [100,101] attempted to condition a motor response in pigeons (walking or running) to the presentation of a magnetic field stimulus ( 5 0 e with a frequency of 120 Hz) produced by a large solenoid. The conditioning procedure was a classical conditioning paradigm involving the presentation of a conditioning stimulus (CS) followed by a shock (unconditioned stimulus, US). The birds were required to make the criterion motor response or conditioned response (CR) prior to US onset and during the CS presentation. Using either a buzzer or a light stimulus as the CS, two pigeons reached a level of 95% conditioning. However, when the magnetic field stimulus was used as a CS, no conditioning was demonstrable. The fact that these authors used a fluctuating magnetic field, rather than a static field, limits generalization to any effects the earth's static field may have on orientation. At best one can conclude that in the procedure used, conditioning to a fluctuating magnetic stimulus was not possible. Meyer and Lambe [93] used an operant conditioning procedure in an attempt to demonstrate that pigeons can discriminate the presence of a magnetic cue. In their procedure, Meyer and Lambe reinforced pigeons on a variable interval reinforcement schedule (VI-1). A magnetic field of 0.56 to 1 Oe was used as the S Dduring the experimental trials, visual cues were used as the S D during control trials. The birds learned to discriminate between the stimulus signalling reinforcement and the stimulus signalling nonreinforcement for the visual S Dbut not for the magnetic S t). Since the magnetic fields used in this study were constant fields with intensities very close to natural levels, these results are much more compelling than those of Orgel and Smith [100,101]. Using a classical conditioning procedure, Reille [117] was able to demonstrate a conditioning of magnetic cues to the cardiac rhythm in pigeons. An increase in heart rate, the unconditioned response, produced by a shock US, was conditioned to the neutral CSs. Reille used three different types of Helmholtz coil produced magnetic stimuli as CSs; a constant field of 0 . 8 0 e and oriented at 120° to the terrestrial field, a fluctuating field of 0.2 to 0.5 Hz and a fluctuating field of 300 to 500 Hz. Although the best conditioning occurred to a light stimulus CS, both the static magnetic field and the

260 fluctuating fields produced conditioning. Using a similar conditioning procedure, Yakovleva and Medvedava [170] also found conditioning of a heart rate response to a high intensity magnetic field stimulus. The CS used was a 520 Oe field created by a horseshoe magnet and the US was the application of ammonia vapour to the birds beak. In 3 out of 5 birds, an increase in the number of conditioned cardiac reactions was observed following application of the magnetic field. Unfortunately, since the field strength used in this study was very high, generalization of these results to those involving geomagnetic cues, is not warranted. Since the paper by Reille [117] seemed to be one of the few studies suggesting that a magnetic field stimulus could achieve control over some response in a pigeon, Kreithen and Keeton [173] attempted to replicate these findings. Using an elaborate setup, these authors were able to control not only the intensity of the applied field, but also the declination and dip angle. Measurements of the resultant field strengths (i.e., the result of imposing the artificial field upon the geomagnetic field) were also made. Using a number of different field strengths, declinations and dip angles, no conditioning of heart rate could be reliably demonstrated when a 10 sec constant field was used as a CS. Although an initial series of experiments suggested a difference between birds exposed to a constant field CS and those exposed to a square wave 0.91 Hz field in terms of response pattern, a subsequent replication attempt using a square wave field of 1.25 Hz, proved negative. Kreithen and Keeton tested a total of 97 pigeons but failed to obtain any consistent conditioning of heart rate to magnetic cues. Beaugrand [9], in a similar series of tests, subjected pigeons to a cardiac orienting reflex test to both magnetic and visual stimuli and then attempted to condition these same stimuli to a change in cardiac activity (UR) elicited by footshock (US). Magnetic cues failed to elicit an orienting reflex and also failed to become conditioned to the cardiac activity changes following footshock. Beaugrand suggests that either there are biological constraints which make conditioning to magnetic cues unlikely within this type of classical conditioning paradigm, or these birds were indeed insensitive to magnetic stimuli. Further cardiac conditioning tests on seven species of European birds also failed to show any positive results [10]. Another attempt to condition magnetic cues to some response in a bird, was made by Emlen [46]; again with negative results. He used an operant conditioning procedure in an attempt to demonstrate magnetic sensitivity in Indigo buntings (Passerina cyanea). In the procedure, an avoidance conditioning technique was employed. Upon the presentation of a CS, the bird was required to hop up onto a perch in order to avoid a shock which followed the CS. Three different types of CSs were used: a buzzer, a change in the ambient magnetic field direction of 180°, or a change of 90°. The magnetic field changes were produced by two Helmholtz coils and the magnetic field intensity was kept at the natural level of 0.55 Oe. When the buzzer was used as a CS, the birds showed an improvement in avoiding shock over trials. No such improvement was seen when either of the two magnetic CSs were used. A recent study [20] demonstrated that pigeons could successfully discriminate between the presence or absence of a magnetic field. The birds were trained to travel down a flight tunnel (housed in a metal room which reduced the natural magnetic field level to 0.02 Oe) and to enter one of two compartments containing food. The absence or presence of a

OSSENKOPP AND BARBEITO magnetic field of 0 . 5 0 e produced by Helmholtz coils provided information as to which goal box contained food. The data showed a significant discrimination by the pigeons on the basis of the magnetic information. Also, Bookman observed that on some trials the birds would engage in "flutter" behavior prior to entering the correct goal box. When the trials in which "flutter" was observed were analyzed separately from the " n o flutter" trials, it was found that a significant discrimination occurred only on the "flutter" trials. The " n o flutter" trials showed chance levels of performance. Thus, this study not only demonstrates that it may be possible to condition pigeon behavior to magnetic cues, but also indicates that increased motor activity ("flutter") may be necessary for conditioning to be successful. Clearly, attempts to condition magnetic cues to various types of arbitrary responses in birds have mainly resulted in negative findings. Although Reiite's [117] positive results were suggestive, subsequent attempts at systematic replication proved negative. The positive results of Bookman [20] are encouraging, especially his finding which suggests that increased motor activity may be necessary for successful conditioning to magnetic cues. However, these positive resuits are in need of replication. Possible reasons tor the large number of negative results obtained by the conditioning procedures will be discussed in a subsequent section.

Systematic changes in orientation behavior Jbllowin~,, magnetic field manipulations. A second and perhaps more cogent method of demonstrating stimulus control by magnetic cues, involves the production of systematic changes in some orientation behavior as a consequence of systematic changes in some characteristic of the ambient magnetic field that might convey directional information. This approach has been visibly more successful in demonstrating stimulus control than have the conditioning studies. The studies which provided the first experimental verification of stimulus control of orientation behavior by a magnetic cue, employed the Kramer-cage method in the study of orientation behavior in European robins [91,161]. By changing the direction of the ambient horizontal magnetic field component in the test area, the birds were induced to change the direction of their motor responses during spring migratory restlessness in a predicted direction. For example, when the magnetic N was changed to a geographic ESE direction, the direction of orientational responses changed from a N E direction (the normal control direction) to an E direction, i.e., a magnetic NNW direction. When the magnetic N was changed to a geographic W direction, orientation changed appropriately to a NW direction (magnetic NE). Similar results were found for experiments done during autumn [156,157]. Systematic changes in both the horizontal intensity and inclination of the applied fields, revealed that the strength of the horizontal component could be varied greatly without influencing the birds' orientation ability, as long as the total intensity of the field remained within certain limits. When the inclination was changed from +66 ° to -66 ° , intensity and north direction remaining constant, the birds changed from their normal spring orientation (NNW) to an opposite orientation (S). Thus, when the inclination was negative (i.e., the vertical component of the field was directed upward such that the angle between the magnetic field lines and the force of gravity was greater than 90°), the birds oriented in a direction opposite to the normal spring migratory direction. Tests varying the inclination in a positive range only (+120 ° to +66 °) showed no effect on direction of orientation [ 156,157]. Wiltschko concluded that only the re-

G E O M A G N E T I S M A N D BIRD O R I E N T A T I O N sultant or total intensity of the magnetic field is important in controlling orientation in European robins; changes in horizontal intensity alone or in declination for positive angles only, had no effect. However, the direction of the vertical component seems to determine the direction of orientation, since opposite directions of the vertical components produce opposite directions in orientation. Similar findings to those found in the European robin, were found also in Garden warblers. Systematic changes in the direction of an imposed magnetic field, produced corresponding changes in the orientation behavior of Garden warblers in Kramer-cages. Also, when a field with an inclination of 0° was provided, random orientation was obtained [1581. Research using the Indigo bunting as the test species also has yielded positive results [49] although the initial indication was that this species was not sensitive to geomagnetic information. Originally, Emlen [46] reported a failure to find a directional preference in caged Indigo buntings when the birds were in a visually " c u e l e s s " chamber that did not disrupt normal geomagnetic field information. This result led Emlen to conclude that Indigo buntings could not use geomagnetic information to ascertain direction. However, Emlen et al. [49] were able to get a statistically significant directional response under a visually limited condition with Indigo buntings and, more importantly, they were able to demonstrate that a shift in the horizontal component of the magnetic field at 120" led to a concomitant shift in the orientation of the buntings. The status of the Indigo bunting's sensitivity to geomagnetic information was further clarified when Emlen found that with reanalysis of his 1970 data, a significant directional preference was found [49]. Some complementary evidence to that provided by the extensive research of Wiltschko and his colleagues, comes from a study by Walcott and Green [152]. These authors equipped homing pigeons with a pair of small Helmholtz coils that were placed about the head of the birds; one coil was worn like a collar, the other fitted on top of the head. The two coils were connected in series with a battery which produced a field of about 0 . 6 0 e around the bird's head. By reversing the direction of current flow (done by reversing the poles of the battery), the direction of imposed magnetic field could be reversed. When two groups of experimental birds were released under sunny skies, both groups showed vanishing directions toward the home loft. Under overcast conditions, birds with the applied field pointing down, vanished predominantly toward home, whereas the group with the field pointing up, oriented away from the home direction. Walcott and Green made some estimations of the net vector of the inclination of the applied field and the earth's field at the test site. They concluded that birds with the applied field pointing up would encounter the smallest angle between the magnetic field vector and gravity when flying north, whereas the reverse would be true of the other group. Thus, the data of Walcott and Green [152], suggest that pigeons were using the direction of the steepest inclination of the field to indicate north. If this is indeed the case, then this would not only explain their own data, but would also be consistent with the findings of Wiltschko [157] and the model presented by Wiltschko and Wiltschko [163,166]. In contrast to the paucity of positive results obtained when stimulus control was attempted using conditioning procedures, this second method involving systematic changes in the applied magnetic field parameters, has proven much more fruitful. Not only orientation behavior during

261 migratory restlessness has been controlled by stimulus manipulation, but also vanishing bearings of homing p~geons. These techniques have probably produced the most compelling demonstrations for the existence of a "magneticcompass".

Ontogenetic Aspects of the "Magnetic-Compass" Research in orientation has been deficient not only in its neglect of developmental aspects, but also in the tack of attention paid to phylogenetic comparisons (cf. [2]). This state of affairs is rather unfortunate, especially when dealing with the search for a magnetic compass, since the basis for a possible sensitivity to magnetic fields has not been pinpointed. Clearly, developmental studies could do much to illuminate the situation. Too, the study of interspecific variation in sensitivity to magnetic fields within a phylogenetic perspective, might shed some light on a possible sensory system. A few scattered studies have dealt with some developmental aspects of the "magnetic-compass" hypothesis. Southern [135] reports some initial experiments involving distortion of the ambient magnetic field during the prenatal development of Ring-billed gull chicks. He placed a pair of crossed bar magnets beneath the nests of incubating gulls (range of the imposed fields was 1 - 2 0 e ) . The eleven chicks which hatched from these nests, were tested in the Southern-type orientation apparatus when 3 days old; control chicks came from undisturbed nests. Normal geomagnetic conditions prevailed during the testing situation which took place under clear skies. Unlike the controls, the experimental chicks showed random orientation. These results suggest that the magnetic field applied during the embryological development of the gull chicks, in some way influenced their ability to use ambient geomagnetic cues for orientation in the post-hatch period. Experiments on some developmental aspects of geomagnetic related orientation in pigeons, were carried out by Keeton [64]. In a series of studies in which magnets were attached to the backs of pigeons, Keeton demonstrated that young inexperienced birds were able to orient homeward only under sunny skies when not wearing magnets. Under overcast conditions, or when wearing magnets, random orientation was obtained (cf. [66]). Thus it seems that very young inexperienced pigeons require both solar and magnetic cues in order to orient appropriately. In experienced birds there is a slight disturbing effect of attached magnets during sunny conditions, when the pigeons are released in unfamiliar territory at large distances [64]. Similar results were obtained using the Walcott technique [151]. The disruption experiments, although suggestive, can only be taken as indirect evidence; only the stimulus control procedure could provide direct evidence of the developmental processes involved in a "magnetic-compass". Unfortunately, no developmental studies have involved the stimulus control procedure of systematic changes in magnetic field parameters. Wiltschko [158,159] has found support for an innate "magnetic-compass" in garden warblers. Handraised warblers that had never seen the stars or the sun were able to orient correctly in a Kramer-cage inside a closed room under normal geomagnetic field conditions. These data show that the maturation of a "magnetic-compass" does not need to be coupled to visual information such as celestial cues, suggesting that it may be innate. However, the possibility that some

262 imprinting like process may be involved is not excluded by these findings. The ontogenetic relationship of a "magnetic-compass'" to other compass systems such as the sun-compass or starcompass, is also of interest. Experiments on European robins showed that when tested under clear sky conditions in a Kramer-cage, the mean direction of the bird's orientation responses was due to magnetic field cues. Under total overcast conditions, orientation responses showed less variance (i.e., were more concentrated) than under partly overcast conditions [160]. The suggestion is made that during migration birds try to transfer their directional information, obtained from geomagnetic cues, to secondary target cues such as star patterns. Moving clouds under partly overcast conditions might interfere with this process. In a series of studies on old world warblers (Syh,ia communis. S. borin and S. cantilhms), Wiltschko and Wiltschko [164] tried to determine the importance birds assign to information from the stars relative to information from the magnetic field. Under clear sky conditions all three species oriented appropriately when the geomagnetic field was normal. When magnetic N was turned by 120° to ESE, all three species used the magnetic cues to orient by, despite contradictory information from stellar cues. When the total intensity of the magnetic field was reduced from 0.42 to 0.32 Oe (inclination of 90°), no significant directional preference was obtained even though the stars were visible. These data strongly suggest that the magnetic field provides the primary source of directional information for these three warbler species, and that stellar cues do not contain directional information in themselves, but that information from the geomagnetic field might be transferred to them. The ecological advantages of such a system are discussed by the authors [ 164]. Similar findings were reported for the European robin [165]. The birds were placed in a test apparatus which allowed a 950 view of the sky around the zenith and the direction of magnetic north was changed. Initially, the birds continued to show their normal orientation, but after approximately three test nights, the robins changed their orientation to agree with the geomagnetic cues. Since a change in orientation is immediate if geomagnetic cues are changed when the robins are in a closed room (e.g., [156,157]), some factor present in this test situation must have provided the robins with directional information that temporarily superseded the magnetic information. Wiltschko and Wiltschko speculated that the directional source was the pattern of stars in the visible portion of the sky, although the process of change from stellar to magnetic cues is not clear. Nevertheless, these findings are in agreement with the results from the Wiltschkos' [164] warbler study and are in agreement with the notion that magnetic information is the basis of the star compass even though the relative importance of these two compass systems may differ among species. If magnetic cues are the primary source of directional information with the celestial and other sources playing a secondary role, then the direction derived from magnetic information should be transferable to other stimuli. This was the basis for a recent study by Wiltschko and Wiltschko [167]. In this study, a random pattern of "stars" (pinpoint sources of light) was used in a laboratory test on European robins. The birds were first tested for orientation within the normal geomagnetic field (0.46 Oe, magnetic north 80°, 48 ° inclination) and the "star" pattern. In the second test for orientation, the magnetic field was one in which random

OSSENKOPP AND BARBEll'() orientation was obtained for a control group (0.32 Oe, magnetic north 360 °, inclination 57°), but the artificial "'star" pattern was present. The mean orientation for the two tests was 83°E and 81°E, respectively. Thus, the robins were able to use a random pattern of pinpoint light sources to determine direction. These data provide fairly conclusive evidence that the magnetic compass is the basis for orientation, at least for the European robin, and that other compass systems are probably secondary in nature and gain their compass characteristics from the "magnetic-compass".

Phylo~,,enetic Aspects o[the "Ma~,,netic-Compas.s'" Relevant to the phylogeny of the "magnetic-compass" are the reports that European robins adjust their sensitivity to the ambient magnetic field when intensities outside their normal range are encountered [156, 157, 160]. Studies indicate that, normally, when this species is subjected to atypical magnetic field intensities random orientation occurs. However, if the birds are first adapted to a deviant field intensity for 3 days or more, they are able to orient correctly. Similar results were obtained for sylvid warblers [161]. Flexibility to adjust the range of sensitivity seems to be of phylogenetic importance for at least two reasons. First, changes in geomagnetic field intensity at a given location occur over time. So, it would seem advantageous for an organism to have a flexible rather than a rigid sensitivity range. And second, the total geomagnetic intensity varies with geographic location, decreasing by more than 5(YE from the poles to the equator. Thus, long distance migrants encounter a variety of field intensities during migration and an adjustable "setpoint" mechanism would allow the birds to reset their compass mechanisms to the local geomagnetic intensities Icf. [166]). Related to the problem of variation in the geomagnetic field intensity are the phylogenetic aspects of the directional component of the compass mechanism. Wiltschko [157] has demonstrated that for European robins and old world warblers, directional information does not depend on the polarity of the geomagnetic field, but rather on the angle between gravity and magnetic field direction. Since there is evidence suggesting that there have been a number of reversals in the polarity of the geomagnetic field since the phylogenetic origins of ayes, a directional mechanism of this sort is not clearly advantageous. A problem with Wiltschko's model of the "magnetic-compass" [157, 158, 163, 166] is its inability to account for transequatorial migrations. Upon crossing the equator, a bird would somehow have to reverse its directional mechanism, since in the southern hemisphere the smaller angle between the field lines and the gravity vector would indicate south, not north. So, given this model, some other compass mechanism or secondary cue system would have to be used to cross the equator. The data available suggests that the "magnetic-compass" evolved in such a manner as to avoid the problems of changes in geomagnetic field intensity and changes in field polarity over time. However, these data are based on only a few avian species, and under specific test conditions. Further experimentation involving a greater number of test species in a wide variety of geographic locations should determine the validity of the "magnetic-compass" model proposed by Wiltschko. Data showing that some invertebrates possess a "magnetic-compass" that functions only within certain field intensities, and that does not seem to depend on field polarity for directional information, suggests that such a

G E O M A G N E T I S M A N D BIRD O R I E N T A T I O N compass mechanism may be a very primitive method of direction finding in all animals. Comparative studies are needed to determine the phylogenetic development of this method of orientation.

Problems, Criticisms and Comments As the foregoing review of the experimental literature indicates, many different approaches have been used in the pursuit of a demonstration that birds can, or can not, use magnetic cues for orientation. Some problems with the research stem from the idealogical approaches of the investigators, other problems are inherent in any study of biological function. Problems related to magnetic field characteristics. The methodology by which bio-effective magnetic field configurations can be determined, is influenced by two approaches. One approach assumes that the stronger the applied stimulus, the stronger or more visible the response elicited or controlled by the stimulus. The other approach emphasizes that " n a t u r a l " magnetic field intensities, frequencies and geometries should be simulated as closely as possible to produce optimal effects [107]. As Persinger has so aptly put it, "there are at least two methods by which a locked door can be opened: by using the appropriate key or by breaking the lock" [107]. However, a door with a broken lock may behave differently from a functional door. The earlier failure to obtain effects when birds were exposed to magnetic fields, can often be attributed to the failure to use the appropriate " k e y " to unlock the behavioral " d o o r " . Experiments using magnetic field intensities substantially above normal field levels (e.g., [69, 100, 101, 102, 170]) may not have been dealing with the same physiological processes as those which occur during exposure to natural intensity magnetic fields. High intensity fields may act as a stress stimulus rather than as a directional stimulus. Similarly, experiments using fluctuating or impulse fields rather than static magnetic fields, may also have been using the wrong " k e y " (e.g., [73, 100, 101, 117]). Indeed, early failures to find effects of wing-magnets on orientation, may have been due to the placement of the magnets. When attached to the wings, a fluctuating magnetic field rather than a static field would be present during flight as a result of the wing movements. Lamotte's failure to obtain disruption of orientation when attaching wing magnets to pigeons, could be explained in this manner [76]. However, this is an empirical question which awaits further examination. The monumental work of Wiltschko and his colleagues clearly shows that at least for some birds, the magnetic " k e y " lies within a critical intensity range and static fields prove quite effective. Interestingly, F. A. Brown's work (e.g., [25]) has demonstrated a comparative critical intensity range for modification of planarian and snail behavior with magnetic fields. Thus there is clear evidence that a " l o c k and k e y " problem may exist and future studies must be cognizant of this factor when investigating the "magneticcompass". The biological "preparedness" problem. Recent research in the areas of psychology and ethology, has found that the equipotentiality premise, stating essentially that any stimulus can be conditioned to any response with equal success, may not be true. In a now classic study, Garcia and Koelling [53] demonstrated that not all stimuli can be conditioned to any response. They expose rats to a taste stimulus and an audiovisual stimulus paired with radiation

263 sickness. Only the taste and not the audiovisual stimuli acquired aversive properties (i.e., were avoided in subsequent tests). On the other hand, rats given these same two types of stimuli but paired with foot shock, only acquired aversion to the audiovisual stimuli, not to the taste. Much subsequent research has reported similar instances of what has been termed "biological preparedness" (for example, see [60,128]). This notion states that certain responses are more likely to be associated with certain stimuli; a result of the organisms phylogenetic history. In light of this principle, the failure to obtain conditioned stimulus control in birds with the use of magnetic cues is no longer surprising. The responses used in these experiments, such as cardiac rhythm or hopping onto a perch, may not be the relevant responses which are "biologically prepared" to occur in the presence of magnetic cues. The success in obtaining stimulus control when using magnetic cues and measuring orientational responses (e.g., [ 152,157]) is consistent with this hypothesis. If this hypothesis holds, the failure to condition magnetic cues to arbitrary responses in birds no longer presents an obstacle to a "magnetic-compass" hypothesis. Related to this " p r e p a r e d n e s s " problem is the role of the physiological " s t a t e " of the animal in the conditioning procedure. It may be the case that magnetic cues can only be discriminated under certain physiological" states". The findings of Bookman [20] seem to suggest that increased motor activity (or perhaps some correlates, e.g., increased metabolic rate) may be a prerequisite for discrimination of magnetic cues by pigeons. The observations by Wiltschko and his group (e.g., [156, 157, 158, 161]) and by Emlen [49] on changes in orientation behavior subsequent to ambient magnetic field changes, are based on measurements of motor behaviors during migratory restlessness; a measure also involving increased motor activity. Thus, the physiological " s t a t e " of the bird may prove to be an important variable controlling the ability of the organism to detect the geomagnetic field. Problems with the dependent variable. A number of criticisms have been made of the methodological and statistical procedures used by Wiltschko's group in investigating the role of magnetic fields in bird orientation. A good review of these criticisms can be found in Emlen [47]. Briefly, a number of researchers have found that if the cage design used in the "Zugunruhe" experiments is altered, the positive results usually found in the Wiltschko studies tend to become statistically nonsignificant. For example, eight-sided cages with radially aligned perches have been used in those experiments obtaining positive results. When the perches are arranged tangentially, a number of researchers have been unable to obtain comparable positive results (e.g., [105,153]; for a good review of this issue, see [62]). Experiments comparing the Emlen "funnel" design cages [48] with the radial-perch cages, indicated that both produced positive resuits, but the radial-perch design results were more clearcut and produced larger differences [47]. Thus, the outcome of these types of experiments depends on the cage design used. A related issue involves the statistical procedures used in the "Zugunruhe" cage experiments. Typically, it is necessary to pool data in order to obtain statistical significance. F o r example, the mean direction of a single bird for a given night is usually used as the raw data and different numbers of birds and different numbers of replications per bird are pooled to obtain an overall mean (cf. [47]). Since such pooling procedures seem to be necessary to obtain statistical significance, many have questioned the usefulness of the

264 data in terms of biological significance. What must be remembered, however, is that statistical significance is a function of the variability present in the data. Data from this type of experiment normally contain a large degree of noise or variability which is probably attributable to the imprecision of the dependent variable. It should be pointed out that the behavior displayed during migratory restlessness or "Zugunruhe" is quite different from actual orientation behavior during flight. Perhaps then, it is not too surprising that a large amount of noise exists in the data from the "Zugunruhe" experiments. The issue thus becomes one of finding a dependent variable that will allow us to discriminate more clearly the effects of the independent variable. The necessity of pooling results to obtain statistical significance may simply be reflecting the inadequacy of the dependent variable and, as such, should not vitiate the existence of an effect of the independent variable. Clearly a search for dependent measures of bird orientation which can better discriminate the effects of magnetic field manipulation is in order. The problem of interspecific variation. Failure to demonstrate sensitivity to magnetic cues in one species of bird, is often presented as evidence against a "magnetic-compass" hypothesis. Indeed, Adler [2] contends that a successful theory of orientation requires a universality of some mechanism. However, comparisons of sensory capacities within a cross-phyletic or intraphyletic perspective could prove beneficial. Much more comparative research in different bird species in terms of magnetic sensitivity and detection, is required. As Skinner [129] has pointed out, an organism's behavior is a consequence of environmental stimuli, both in the ontogenetic as well as in the phyiogenetic sense. Magnetic cues would clearly be of different salience to different species of birds throughout their evolutionary history. The problem of alternate orientational cues. Related to the specific variation problem is the possible occurrence of a hierarchy of orientational mechanisms in the same bird. The central issue in this problem is the question of the relationship among the various proposed compass mechanisms (i.e., sun-compass, star-compass, "magnetic-compass," etc.). Wiltschko has argued that the "magnetic-compass" is the ontogenetic basis (and perhaps phylogenetic basis) for all other compass mechanisms [167]. On the other hand, it is conceivable that several compass mechanisms evolved independently of one another and have a complex interrelationship; the predominance of a given mechanism depending on situational cues. For example, the data showing that pigeons with attached magnets can orient under sunny skies has been presented as evidence for a hierarchy of orientation mechanisms in birds; the sun-compass being preferentially used over the "magnetic-compass" [65]. However, this finding is not inconsistent with Wiltschko's suggestion that the starcompass and sun-compass are based on the "magneticcompass". Thus what remains to be resolved is the degree of interdependence among the various compass systems. Related to the above problem is the issue of the sensory capabilities of the test species. Researchers must be aware of the sensory capabilities of the species being tested and control for possible cues interfering or interacting with the mechanism they are investigating. Recent findings that pigeons are sensitive to polarized light [74] and very small changes in atmospheric pressure [75] makes the admonishment that the sensory capabilities of the test organism should be known as accurately as possible, all the more urgent. The problem of a mechanism for a biomagnetic effect. The failure to find the biophysical mechanism which allows

O S S E N K O P P AND BARBEITO an animal to sense or detect magnetic field parameters is perhaps the greatest obstacle to the acceptance of the "magnetic-compass" hypothesis. Few scientists are willing to accept an interaction between a stimulus and an organism, at the level of information transfer, without knowing what sensory mechanism is involved. Clearly, the search for a biomagnetic sensory apparatus within the organism is of top priority not only for research within the area of bird orientation but within the general area of environmental psychobiology. The research demonstrating a biomagnetic effect in other animals, suffers from the same problem. However, the data presented in this review along with the data on other animals, certainly warrant an intense effort to find the biomagnetic mechanism. Alternative explanations to that of a biological effect of magnetic fields can no longer explain the positive demonstrations accumulated to date.

THEORETICAL ISSUES

Models of Biomagnetic Sensitivity Although the weight of the evidence dealing with possible biological effects of magnetic fields is positive, the mechanism(s) whereby such effects are produced, remain to be found. Finding the " s e n s o r y system" used in detecting magnetic fields seems to be difficult for several reasons. Unlike most energy forms sensed by conventional sensory mechanisms, magnetic lines of force can pass right through biological tissue. Thus, the "magnetic sensory system" does not have to be peripherally located; it could be in any organ of the body, such as in the brain, or it could be a distributed system. In addition, no biophysical mechanism for an effect of magnetic fields on cellular or subcellular components has been demonstrated; pinpointing this biophysical mechanism would be a first step in finding the magnetic sensory apparatus. Barnothy [7] has listed up to 20 kinds of interactions that are theoretically possible between a constant magnetic field and various processes in biological tissue. These interactions can generally be divided into microscopic or macroscopic effects [114]. For the microscopic effects the assumption is that the biomagnetic mechanism is a physical one induced at the molecular or even atomic level. The orientation of molecular spins, the orientation of diamagnetic or paramagnetic molecules, or even the valence angles in molecules could be altered by imposed magnetic fields. At the macroscopic level, effects such as changes in the rotation rate of erythrocytes [99] or rotation and alignment of suspended retinal rod cells [38] when placed in magnetic fields. have been proposed and described (cf. [114]). Other possible mechanisms include the Hall effect (the voltage generated perpendicularly to a current flowing across a magnetic field) and magneto-resistance. Unfortunately, all of the above mechanisms require high intensity fields (several thousand Oe) to produce appreciable biomagnetic effects (cf. [40]) and would therefore seem to be unlikely candidates for a biomagnetic mechanism with sensitivity to magnetic fields in the order of 0.5 Oe or less. More attractive speculations about the biomagnetic mechanism are presented by Russo and Caldwell [124] and Cope [40]. Russo and Caldwell suggest that the neuroglial complex in the central nervous system can behave like a P-N semiconductor. Semiconductors are made of crystalline substances into which impurities have been introduced to

G E O M A G N E T I S M A N D BIRD O R I E N T A T I O N alter their electrical properties. Two crystals of the same substance but with different impurities and therefore different electrical properties, make up a P-N semiconductor. These devices have the properties of ionic barriers, directional control of current, power amplification and susceptibility to magnetic induction. An external magnetic field can induce a current within a semiconductor moving within the field. However, unlike conductors where currents can be induced in either direction, the biasing function in semiconductors will permit current induction in one direction only. Glial and neuronal membranes show an ordered structure (liquid crystal) but differ in electrical properties [144] thus allowing for the possibility that they display semiconductor properties including sensitivity to ambient magnetic fields. A second mechanism, proposed by Cope [40], is based on the Josephson junction concept. The Josephson junction consists of two layers of a superconductor, separated by a thin layer of dielectric substance. A tunneling current of Josephson current across the junction is markedly reduced by very weak magnetic fields due to electron interference effects. The properties of the Josephson junction that are of interest are: a marked effect of temperature, the property that the effect of a magnetic field on the Josephson current is the same when the direction or polarity of the magnetic field is reversed, and small changes in magnetic fields may produce a large percentage change in Josephson current. Evidence for super conduction of organic molecules at high temperature and for superconduction in living systems due to threshold magnetic field effects, has been reviewed by Cope [39].

Models of the Magnetic Sensory Mechanism in Birds More specific models dealing with magnetic field detection and use during bird orientation, have also been proposed. Yeagley [171], Barnothy [6] and Talkington [139,140] have all hypothesized detection of the geomagnetic field via electromotive forces induced in a bird when flying through the field (the Hall effect). However, Keeton [64] has calculated that even in an optimal situation the most optimistic estimate of the induced electromotive force is in the order of 1 mV per cm. Keeton suggests that " a n estimate on the order of 1 /xV per cm is probably more realistic for the required sensitivity of the bird's sensory apparatus if directional information is to be obtained." In addition, the electric fields induced by the magnetic field could probably not be discriminated from the earth's electrostatic field which is in the order of 1 V per cm and quite variable (cf. [42, 130, 147]). Finally, the demonstration that even stationary birds can appropriately alter their orientation when the ambient magnetic field direction is changed (e.g., [157]) certainly is not consistent with any model requiring that the bird be in flight in order to detect the geomagnetic field. Stewart [137] has suggested a model based on a different principle. When flying through the air, a bird will build up an electrostatic field on its surface as a result of moving through the atmospheric electric field. An electric charge surrounded by its own magnetic field and moving within another magnetic field will be affected by the interaction of the two magnetic fields. Therefore, a flying bird with its own electrostatic field will have a torque acting on it as a result of the interaction of the magnetic component of its electrostatic field with the geomagnetic field. Under optimum conditions the calculated torque would be in the order of only 1 dyne. Although

265 this force is perhaps rather small to be detected by the bird, the demonstration by Tanner and Romero-Sierra [142] that feathers exhibit piezoelectric properties, makes this model more plausible. When exposed to electric stress feathers twist, with the degree of twist being proportional to the strength of the electrical excitation. Receptors in the feather sockets could conceivably measure the amount of twist and in some way enable the bird to measure both the electrostatic field on its feathers and the ambient magnetic field. The data detracting from such a model are, again, the demonstrations that a stationary bird can change its orientation subsequent to changes in the ambient magnetic field direction. One would not expect much of an electrostatic field to accumulate on the surface of a stationary bird. Too, such specialized structures as the piezoelectric properties of feathers, are inconsistent with a cross phyletic sensitivity to magnetic fields. It is perhaps interesting to compare the empirical data on bird orientation in magnetic fields with the above proposed models of biomagnetic sensitivity. Clearly, the data provided by studies in which the birds were in flight, as well as the data yielded by studies in which the birds were not flying (e.g., [133,157]) must be explained by the model. In addition, the model must account for the data of Wiltschko and Wiltschko [163] showing that orientating birds do not use the polarity of the magnetic field to tell direction, but rather determine " n o r t h " as the direction where the magnetic field lines and the gravity vector form the smaller angle. The model most consistent with these data is the biological superconductive Josephson junction model. It would not only have the required sensitivity (cf. [40]) but also is consistent with the Wiltschko and Wiltschko data; the Josephson junction does not differentiate the polarity of the ambient magnetic field. Although the consistency of this model with the data does not prove that this model is correct, such consistency should not go unnoticed. Most recently Leask [79] has suggested a mechanism of magnetic field detection based on an optical pumping mechanism which takes place in the bird's eye, in the molecules of the retina, as an adjunct to the normal processes of vision. Predictions made from this model also fit the data well enough to indicate that further study of this proposal is warranted, even though some of the model's assumptions are speculative.

SUMMARY A N D C O N C L U S I O N

Summary The data collected to demonstrate the existence of a "magnetic-compass" used in bird orientation, are not always consistent and are often of a "statistical" nature, i.e., the relationships are often not obvious. The following points may be viewed as comprising the characteristics of the positive evidence. (1) Magnetic fields have been shown to have a biological effect on a variety of life forms ranging from unicellular organisms to man. Although many of these demonstrations have involved high intensity magnetic fields (>1000 Oe), a good number of studies have used near natural field levels (<10e). (2) Magnetic fields have been shown to have an effect on orientation behavior for many animals other than birds. Included among those animals showing changes in orientation subsequent to changes in the ambient magnetic field char-

266

OSSENKOPP AND BARBEITO

acteristics are planaria, flies, termites, honeybees and goldfish. (3) Indirect methods of demonstrating the existence of an avian magnetic-compass have been successful. Effective methods of disrupting the compass mechanism include attaching magnets to the head or body of birds during orientation tasks, placing the bird within an artificial magnetic field created by Helmholtz coils, and shielding out the geomagnetic field or distorting it. In addition, natural disturbances in the geomagnetic field called magnetic storms, have been shown to disrupt orientation behavior in some birds. (4) More direct methods of demonstrating the existence of a "magnetic-compass" also have been successful. Stimulus control using magnetic stimuli, has been effective when orienting responses of birds were investigated. Systematic changes in some orienting behavior as a consequence of systematic changes in the direction of the ambient magnetic field, have been shown in several different species and for several different types of responses. While attempts to gain stimulus control over some seemingly arbitrary response in birds via magnetic cues have been largely unsuccessful, it may well be the case that the criterion response was not conditionable to magnetic stimuli. Only recently have researchers begun to look beyond the singular question of the existence of a " m a g n e t i c - c o m p a s s " ; thus, very little is known about the characteristics of the compass mechanism, or its role in the overall picture of avian orientation. Although recent investigations into the compass mechanism indicate that European robins and old world warblers do not use the polarity of the magnetic field to tell direction but take the direction for north where the field lines and the gravity vector form the smaller angle, the generality of these data is questionable. And while recent work suggests that magnetic cues are the primary source for directional information with the other compass systems being secondary sources, it is not clear that all the homing pigeon data can be explained in this manner. Extensive investigation of the characteristics of the "magnetic-compass" is only now beginning and much more research is needed before its ontogeny and phylogeny is understood. Conclusions and Suggestions

The history of the "magnetic-compass" hypothesis has

been uncertain and the research has often been poorly designed and/or poorly conducted---leading to inconclusive results. Only recently has more systematic attention been paid to this area. To date, the main thrust of the research in this area was directed at either proving or disproving the existence of a "magnetic-compass". From the data reviewed in this paper, the conclusion can be drawn that at least some avian species possess a "magnetic-compass". It would therefore seem appropriate that future research no longer direct its attention solely to showing the existence of a "magnetic-compass" but rather to investigating the nature of this compass mechanism. Once the existence of a "magnetic-compass" is accepted, questions concerning various aspects of the compass mechanism press into prominence. Of foremost importance among these questions are those concerned with the biophysical mechanism by which magnetic fields interact with biological tissue. Only by finding the site and method of operation of the "magnetic-compass" system can i! be brought under laboratory control and its properties investigated. Other important questions concern the ontogeny of this compass mechanism, since many of our experimental problems stem from the lack of knowledge in this area. Knowing how the "magnetic-compass" interacts with other compass systems is necessary for the design of appropriate control groups in many experiments. Too, knowledge about the ontogeny of this compass system may give us some clues as to the underlying biophysical mechanism. In addition to questions concerning the compass mechanism itself, attention should also be directed at certain methodological difficulties. The types of behavior that can be influenced by magnetic field changes need better definition. Only by doing this can it be determined which responses are most likely to be conditionable to magnetic cues or brought under the control of magnetic stimuli. Concomitantly, parametric studies of various characteristics of the ambient magnetic field and their systematic change in terms of resulting changes in orienting behavior are also necessary. Finally, the above-mentioned considerations must be directed at a wider base of avian species. Research in this area deals with too few species and a more comparative approach is necessary in order to establish the limits of generality of the "magnetic-compass" phenomenon.

REFERENCES

1. Able, K. P. Environmental influences on the orientation of free-flying nocturnal migrants. Anita. Behav. 22: 224-238, 1974. 2. Adler, H. E. Ontogeny and phylogeny of orientation. In: Development and Evolution of Behavior, edited by L. R. Aronson, E. Tobach, D. S. Lehrman and J. S. Rosenblatt. San Francisco: W. H. Freeman and Co., 1970, pp. 303-336. 3. Akoev, B. N., O. B. Ilyinsky and P. M. Zadan. Responses of electroreceptors (ampullae of Lorenzini) of skates to electric and magnetic fields. J. comp. Physiol. 106: 127-134, 1976. 4. Andrianov, G. N., G. R. Brown and O. B. Ilyinsky. Responses of central neurons to electric and magnetic stimuli of the ampullae of Lorenzini in the black sea skate. J. comp. Physiol. 93: 287-299, 1974. 5. Aymar, G. C. Bird Flight. New York: Dodd, Mead, 1935. 6. Barnothy, J. M. Proposed mechanisms for the navigation of migrating birds. In: Biological Effects of Magnetic Fields, Vol. 1, edited by M. F. Barnothy. New York: Plenum Press, 1964, pp. 287-293. 7. Barnothy, M. F. (Ed.). Biological Effects of Magnetic Fields, Vol. 1. New York: Plenum Press,1964.

8. Barnwell, F. H. and F. A. Brown. Responses ofplanarians and snails, ln: Biological Effects of Magnetic Field~, (Vol. 1). edited by M. F. Barnothy. New York: Plenum Press. 1964, pp. 263-278. 9. Beaugrand, J. P. An attempt to confirm magnetic sensitivity in the pigeon. Colurnba livia. J. comp. Physiol. 110: 343-355, 1976. 10. Beaugrand, J. P. Test of magnetic sensitivity in seven species of european birds using a cardiac nociceptive conditioning procedure. Behav. Proc. 2:113-127, 1977. 11. Becker, G. Ruheeinstellung nach der Himmelsrichtung, eine Magnetfeld-Orientierung bei Termiten. Naturwissenscht~ften 50: 455, 1963. 12. Becker, G. Magnetfeld-Orientierung yon Dipteren. Naturwissenschaften 50: 664, 1963. 13. Becker, G. Reaktion yon Insekten auf Magnetfelder, elektrische Felder und Atmospherics. Z. angew. Entomol. 54: 75-88, 1964. 14. Becker, G. Magnetfeld-Einfluss auf die Galeriebau-Richtung bei Termiten. Naturwissenschaften 58: 60, 1971.

GEOMAGNETISM

AND BIRD ORIENTATION

15. Becker, G. Einfluss des Magnetfelds auf das Richtungsverhalten von Goldfischen. Naturwissenschaften 61: 220-221, 1974. 16. Becker, G. and U. Speck. Untersuchungen fiber die Magnetfeld-Orientierung von Dipteren. Z. vergl. Physiol. 49: 301-340, 1964. 17. Blakemore, R. Magnetotactic bacteria. Science 190: 377-379, 1975. 18. Bliss, V. L. and F. H. Heppner. Circadian activity rhythm influenced by near zero magnetic field. Nature, Lond. 261: 411-412, 1976. 19. Bochenski, S., M. Dylewska, J. Gieszczykiewicz and L. Sych. Homing experiments on birds. Part XI. Experiments with swallows Hirundo rustica L. concerning the influence of earth magnetism and partial eclipse of the sun on their orientation. Pr. Zoo/. pol. pan'st. Muz. przyr. 5: 125-130, 1960. 20. Bookman, M. A. Sensitivity of the homing pigeon to an earthstrength magnetic field. Nature, Lond. 267: 340-342, 1977. 21. Branover, G. G., A. S. Vasil'yev, S. I. Gleiser and A. B. Tsinober. A study of the behavior of eels in natural and artificial magnetic fields and an analysis of its reception mechanism. J. lchthyol. 11: 608-614, 1971. 22. Brown, F. A. Response to pervasive geophysical factors and the biological clock problem. Cold Springs Harb. Symp. quant. Biol. 25: 57-71, 1960. 23. Brown, F. A. Response of the planarian, Dugesia, and the protozoan, Paramecium, to very weak horizontal magnetic fields. Biol. Bull. 123: 264-281, 1962. 24. Brown, F. A. How animals respond to magnetism. Discovery 24(11): 18--22, 1963. 25. Brown, F. A. Effects and after-effects on planarians of reversals of the horizontal magnetic vector. Nature, Lond. 209: 533-535, 1966. 26. Brown, F. A. Some orientational influences of nonvisual, terrestrial electromagnetic fields. Ann. N.Y. Acad. Sci. 188: 224-241, 1971. 27. Brown, F. A., F. H. Barnwell and H. M. Webb. Adaptation of the magneto-receptive mechanism of mud-snails to geomagnetic strength. Biol. Bull. 127: 221-231, 1964. 28. Brown, F. A., M. F. Bennett and H. M. Webb. A magnetic compass response of an organism. Biol. Bull. 119: 65-74, 1960. 29. Brown, F. A., W. J. Brett, M. F. Bennett and F. H. Barnwell. Magnetic response of an organism and its solar relationships. Biol. Bull. 118: 367-381, 1960. 30. Brown, F. A. and Y. H. Park. Duration of an after-effect in planarians following a reversed horizontal magnetic vector. Biol. Bull. 128: 347-355, 1965. 31. Brown, F. A. and Y. H. Park. Association-formation between photic and subtle geophysical stimulus patterns---a new biological concept. Biol. Bull. 132: 311-319, 1967. 32. Brown, F. A., H. M. Webb and F. H. Barnwell. A compass directional phenomenon in mud-snails and its relation to magnetism. Biol. Bull. 127: 206--220, 1964. 33. Brown, F. A., H. M. Webb, F. M. Bennett and F. H. Barnwell. A diurnal rhythm in response of the snail Ilyoanassa to imposed magnetic fields. Biol. Bull. 117: 405-406, 1959. 34. Brown, F. A., H. M. Webb and W. J. Brett. Magnetic response of an organism and its lunar relationships. Biol. Bull. 118: 382392, 1960. 35. Brown, G. R., G. N. Andrianov and O. B. Ilyinsky. Magnetic field perception by electroreceptors in the black sea skates. Nature, Lond. 249: 178-179, 1974. 36. Brown, J. E. The "pigeon cooker". Radio News. 21(4): 60-61, 1938. 37. Casamajor, J. Le mysterieux "sens de l'espace". Rev. Scient. 65: 554-565, 1927. 38. Chalazonitis, N., R. Chagneux and A. Arvanitaki. Rotation des segments externes des photorecepteurs dans le champ magnetique constant. C. r. hebd. Sernc. Acad. Sci., Paris 271: 130-133, 1970. 39. Cope, F. W. Evidence from activation-energies for superconductive tunneling in biological-systems at physiological temperatures. Physiol. Chem. Phys. 3: 403-410, 1971.

267 40. Cope, F. W. Biological sensitivity to weak magnetic fields due to biological superconductive Josephson junctions? Physiol. Chem. Phys. 5: 173-176, 1973. 41. Darling, J. R. Miracles on wings. Nat. Hist., N. Y. 46: 205-207, 240-243, 1940. 42. Davis, L. Remarks on: "The physical basis of bird navigation." J. appl. Physiol. 19: 307-308, 1948. 43. Dorst, J. The Migration o f Birds. Cambridge: The Riverside Press, 1961. 44. Eastwood, E. Radar Ornithology. London: Methuen and Co., Ltd., 1967. 45. El'Darov, A. L. and Y. A. Kholodov. The effect of a constant magnetic field on the motor activity of birds. Zh. Obsch. Biol. 25: 224-229, 1964. 46. Emlen, S. T. The influence of magnetic information on the orientation of the Indigo Bunting, Passerina cyanea. Anim. Behav. 18: 215-224, 1970. 47. Emlen, S. T. Migration: Orientation and navigation. In: Avian Biology, Vol. 5, edited by D. S. Farner and J. R. King. New York: Academic Press, 1975, pp. 129-219. 48. Emlen, S. T. and J. T. Emlen. A technique for recording migratory orientation of captive birds. Auk 83: 361-367, 1966. 49. Emlen, S. T., W. Wiltschko, N. J. Demong, R. Wiltschko and S. Bergman. Magnetic direction finding: Evidence for its use in migratory Indigo Buntings. Science 193: 505-508, 1976. 50. Frei, U. and G. Wagner. Die Anfangsorientierung von Brieftauben im erdmagnetisch gestrrten Gebiet des Mont Jorat. Rev. suisse Zool. 83: 891-897, 1976. 51. Friedman, H., R. O. Becker and C. H. Bachman. Effects of magnetic fields on reaction time performance. Nature, Lond. 213: 949-950, 1967. 52. Fromme, H. G. Untersuchungen fiber das Orientierungsvermrgen nhchtlich ziehender Kleinv6gel (Erithacus rubecula, Sylvia communis). Z. Tierpsychol. 18: 205-220, 1961. 53. Garcia, J. and R. A. Koelling. Relation of cue to consequence in avoidance learning. Psychon. Sci. 4: 123-124, 1966. 54. Gerdes, K. i3ber das Heimfindeverm6gen von Lachmrwen. Verh. dt. zool. Ges. 24: 171-181, 1960. 55. Gerdes, K. Richtungstendenzen von Brutplatz verfrachteter Lachm6wen (Larus ridibundus L.) unter Ausschluss visueller Gel~inde-und Himmelsmarken. Z. wiss. Zool. 166: 352-410, 1962. 56. Gordon, D. A. Sensitivity of the homing pigeon to the magnetic field of the earth. Science 108:710-711, 1948. 57. Graue, L. C. Initial orientation in pigeon homing related to magnetic contours. Am. Zool. 5: 704, 1965. 58. Griffin, D. R. Bird navigation. Biol. Rev. 27: 359-400, 1952. 59. Griffin, D. R. Bird navigation. In: Recent Studies in Avian Biology, edited by A. Wolfson. Urbana: University of Illinois Press, 1955, pp. 154-197. 60. Hinde, R. A. and J. Stevenson-Hinde (Eds.). Constraints on Learning: Limitations and Predispositions. New York: Academic Press, 1973. 61. Hochbaum, H. A. Travels and Traditions o f Waterfowl. Newton: C. T. Branford Co., 1960. 62. Howland, H. C. Orientation of European robins to Kramer cages. Z. Tierpsychol. 33: 295-312, 1973. 63. Keeton, W. T. Magnets interfere with pigeon homing. Proc. natn. Acud. Sci., U.S.A. 68: 102-106, 1971. 64. Keeton, W. T. Effects of magnets on pigeon homing. In: Animal Orientation and Navigation, edited by S. R. Galler, K. Schmidt-Koenig, G. J. Jacobs and R. E. Belleville. Washington, D.C.: U.S. Government Printing Office, 1972, pp. 579-594. (NASA SP-262). 65. Keeton, W. T. The orientational and navigational basis of homing in birds. In: Advances in the Study o f Behavior, Vol. 5, edited by D. S. Lehrman, R. Hinde and E. Shaw. New York: Academic Press, 1974, pp. 47-132. 66. Keeton, W. T. and A. Gobert. Orientation by untrained pigeon requires the sun. Proc. natn. Acad. Sci. U.S.A. 65: 853-856, 1970.

268 67. Keeton, W. T., T. S. Larkin and D. M. Windsor. Normal fluctuations in the earth's magnetic field influence pigeon orientation. J. comp. Physiol. 95: 95-103, 1974. 68. Knorr, O. A. The effect of radar on birds. Wilson Ball. 66: 264, 1954. 69. Knutson, T. The effect of an electromagnetic field on early embryogenesis in Quail. Trans. Iowa Aead. Sei. 76: 510-516, 1969. 70. Kramer, G. Uber Richtungstendenzen bei der n/ichtlichen Zugunruhe gek~Lfigter Vrgel. In: Ornithologie als Biologische Wissenschaft, edited by E. Mayr and E. Sch~iz. Heidelberg: Winter, 1949, pp. 26%283. 71. Kramer, G. Eine neue Methode zur Erforschung der Zugorientierung und die bisher damit erzielte Ergebnisse. Proc. Inter. Ornithol. Cong., Uppsala, 1951, pp. 271-280. 72. Kramer, G. Die Sonnenorientierung der V6gel. Verh. dt. Zool. Ges. 1952, 1953, pp. 72-84. 73. Kreithen, M. L. and W. T. Keeton. Attempts to condition homing pigeons to magnetic stimuli. J. eomp. Physiol. 89: 355-362, 1974. 74. Kreithen, M. L. and W. T. Keeton. Detection of changes in atmospheric pressure by the homing pigeon, Columba livia. J. comp. Physiol. 89: 73-82, 1974. 75. Kreithen, M. L. and W. T. Keeton. Detection of polarized light by the homing pigeon, Columba livia. J. comp. Physiol. 89: 83-92, 1974. 76. Lamotte, M. M. The influence of magnets and habituation to magnets on inexperienced homing pigeons. J. comp. Physiol. 89: 37%389, 1974. 77. Larkin, R. P. and P. J. Sutherland. Migrating birds respond to project Seafarer's electromagnetic field. Science 195: 777-779, 1977. 78. Larkin, T. S. and W. T. Keeton. Bar magnets mask the effect of normal magnetic disturbances on pigeon orientation. J. eomp. Physiol. 110: 227-231, 1976. 79. Leask, M. J. M. A physicochemical mechanism for magnetic field detection by migratory birds and homing pigeons. Nature, Lond. 267: 144-145, 1977. 80. Lindauer, M. Orientierung der Tiere. Verh. dr. zool. Ges. 1976, pp. 156-183. 81. Lindauer, M. and H. Martin Die Schwereorientierung der Bienen unter dem Einfluss des Erdmagnetfeldes. Z. vergl. Physiol. 60: 219-243, 1%8. 82. Lindauer, M. and H. Martin. Magnetic effect on dancing bees. In: Animal Orientation and Navigation, edited by S. R. Galler, K. Schmidt-Koenig, G. J. Jacobs and R. E. Belleville. Washington, D.C.: U.S. Government Printing Office, 1972, pp. 55%567. (NASA SP-262). 83. Llaurado, J. G., A. Sances and J. H. Battocletti. Biological and Clinical EfJects o f Low-Frequency Magnetic and Electric Fields. Springfield: C. C. Thomas, 1974. 84. Martin, H. and M. Lindauer. Orientierung in Erdmagnetfeld. Fortschr. Zool. 21: 211-228, 1976. 85. Martin, H. and M. Lindauer. Der Einfluss des Erdmagnetfeldes auf die Schwereorientierung der Honigbiene (Apis mellifica). J. eomp. Physiol. 122: 145-187, 1977. 86. Matthews, G. V. T. The experimental investigation of navigation in homing pigeons. J. exp. Biol. 28: 508-536, 1951. 87. Matthews, G. V. T. An investigation of homing ability in two species of gulls. Ibis 94: 243-264, 1952. 88. Maurain, C. Les proprietes magnetiqnes et electriques terrestres et la faculte d'orientation du Pigeon voyageur. Nature, Paris 54: 44-45, 1926. 89. McCleave, J. D., E. H. Albert and W. E. Richardson. Perception and effects o f locomotor activity in American eels and atlantic" sahnon o f extremely low frequency electric and magnetic" fields. (Office of Naval Research Contract No. N00014-72-C-0130, 1974.) Orono, Maine: Maine University, 1974. (NTIS No. AD-778 021). 90. McCleave, J. D., S. A. Rommel and C. L. Cathcart. Weak electric and magnetic fields in fish orientation. Ann. N.Y. Aead. Sei. 188: 270-282, 1971.

OSSENKOPP AND BARBEII'O

91. Merkel, F. W. and W. Wiltschko. N/ichtliche Zugunruhe und Zugorientierung bei Kleinvrgeln. Verh. dt. zool. Ge.s. Jena. 1965, 1965, pp. 356-361. 92. Meyer, M. E. Stimulus control for bird orientation. P~vch,d. Bull. 62: 165-179, 1964. 93. Meyer, M. E. and D. R. Lambe. Sensitivity of the pigeon to changes in the magnetic field. Psyehon. Sci. 5: 34%350, 1%6. 94. Moore, F. R. Influence of solar and geomagnetic stimuli on the migratory orientation of Herring gull chicks. Aak 92: 655-664, 1975. 95. Moore, F. R. Geomagnetic disturbance and orientation of nocturnally migrating birds. Science 196: 682-684, 1977. 96. Nahas, G. G., H. Boccalon, P. Berryer and B. Wagner. Effects in rodents of a l-month exposure to magnetic fields (200-1200 Gauss). Aviat. Space Envir. Med. 46:1161-1163, 1975. 97. Neaga, N. and M. Lazar. Histological changes in the thyroids of chicks after treatment with a pulsing magnetic field. Stud. Cere. Biol. Set'. Zool. 24: 11%124, 1972. 98. Nelson, J. H., L. Hurwitz and D. G. Knapp. MagnetLwtl qj'the Earth. Washington, D.C.: U.S. Government Printing Office, 1962. (Publication 40-1). 99. Neurath, P. W. Simple theoretical models for magnetic interactions with biological units. In: Biological Effects qfMagnetie Fiehls, Vol. 1, edited by M. F. Barnothy. New York: Plenum Press, 1964. 100. Orgel, A. R. and J. C. Smith. Test of the magnetic theory of homing. Science 120: 891-892, 1954. 101. Orgel, A. R. and J. C. Smith. A test of the magnetic theory of homing in pigeons. J. genet. Psychol. 88: 203-210, 1956. 102. Ossenkopp, K.-P. and L. J. Shapiro. Effects of prenatal exposure to a 0.5 Hz low-intensity rotating magnetic field on White Peking ducklings. Am. Zool. 12: 650, 1972. 103. Ozhigova, A. P. and J. E. Ozhigov. Constant magnetic field effect on paramecium movement. Biofizika 11: 1026-1033, 1966. 104. Palmer, J. D. Organismic spatial orientation in very weak magnetic fields. Nature, Lond. 198: 1061-1062, 1963. 105. Perdeck, A. C. Does navigation without visual cues exist in Robins? Ardea 51: 91-104, 1963. 106. Persinger, M. A. (Ed.). ELF and VLF Electromagnetic Fiehl EfJ~wts. New York: Plenum Press, 1974. 107. Persinger, M. A. Effects of magnetic fields on animal behavior. In: Progress in Animal Biometeorology, edited by H. D. Johnson. Amsterdam: Swets and Zeitlinger, 1975. 108. Persinger, M. A., H. W. Ludwig and K.-P. Ossenkopp. Psychophysiological effects of extremely low frequency electromagnetic fields: A review. Percept. Mot. Skills 36: 11311159, 1973. (Monograph Supp. 3-V36). 109. Persinger, M. A., G. B. Glavin and K.-P. Ossenkopp. Physiological changes in adult rats exposed to an ELF rotating magnetic field. Int. J. Biometeor. 16: 163-172, 1972. 110. Phillips, J. B. Use of the earth's magnetic field by orienting cave salamanders (Euryeea Lue([uga). J. eomp. Physiol. 121: 273-288, 1977. 111. Picton, H. D. Some responses of Drosophila to weak magnetic and electrostatic fields. Nature, Lond. 211: 303-304, 1966. 112. Poor, H. H. Birds and radar. Auk 63: 631, 1946. 113. Porumb, S. The influence of an electromagnetic field on glucose-6-phosphate dehydrogenase activity in rabbit red blood cells. Stud. Cere. Biol. Set'. Zool. 23: 23%242, 1971. 114. Presman, A. S. Electromagnetic Fields and Life. New York: Plenum Press, 1970. 115. Rabol, J. The orientation of night-migrating passerines without the directional influence of the starry sky and/or the earth magnetic field. Z. 7)'erpsychol. 38: 251-266, 1975. 116. Ratner, S. C. and J. W. Jennings. Magnetic fields and orienting movements in mollusks. J. comp. physiol. Psychol. 65: 365368, 1968. 117. Reille, A. Essai de mise en evidence d'une sensibilite du pigeon au champ magnetique a l'aide d'un conditionnement nociceptif. J. Physiol., Paris 60: 85-92, 1%8.

GEOMAGNETISM

AND BIRD ORIENTATION

118. Richardson, W. J. Spring migration and weather in eastern Canada: A radar study. Am. Birds 25: 684--690, 1971. 119. Richardson, W. J. Spring migration over Puerto Rico and the western Atlantic: A radar study. Ibis 116: 172-193, 1974. 120. Richardson, W. J. Autumn migration over Puerto Rico and the western Atlantic: A radar study. Ibis 118: 30%332, 1976. 121. Riper, W. V. and E. R. Kalmbach. Homing not hindered by wing magnets. Science 115: 577-578, 1952. 122. Rommel, S. A. and J. D. McCleave. Sensitivity of American eels (Anguilla rostrata) and Atlantic salmon (Salmo salar) to weak electric and magnetic fields. J. Fish. Res. Bd. Can. 30: 657-663, 1973. 123. Rubens, S. M. Cube-surface coil for producing a uniform magnetic field. Rev. Sci. lnstrum. 16: 243-245, 1945. 124. Russo, F. and W. E. Caldwell. Biomagnetic phenomena: Some implications for the behavioral and neurophysiological sciences. Genet. Psychol. Monogr. 84: 177-243, 1971. 125. Schneider, F. Beeinflussung der Aktivit/it des Maikafers durch Ver~inderung der gegenseitigen Lage magnetiscber and elektrischer Feldern. Mitt. Schweiz. ent. Ges. 33: 223-237, 1961. 126. Schneider, F. Orientierung und Aktivitiit des Maik/ifers unter dem Einfluss richtungsvariabler kiinstlicher elektrischer Felder and weiterer ultraoptischer Bezugssysteme. Mitt. Schweiz. ent. Ges. 36: 1-26, 1%3. 127. Schneider, F. Ultraoptische Orientierung des Maik~ers (Melontha vulgaris F.) in kiinstlichen elektrischen und magnetischen Feldern. Ergebn. Biol. 26: 147-157, 1963. 128. Seligman, M. E. P. and J. L. Hager. Biological Boundaries o f Learning. New York: Appleton-Century-Crofts, 1972, p. 480. 129. Skinner, B. F. The phylogeny and ontogeny of behavior. Science 153: 1205--1213, 1%6. 130. Slepian, J. Physical basis of bird navigation. J. appl. Physiol. 19: 306, 1948. 131. Southern, W. E. Orientation behavior in Ring-biUed gull chicks and fledgelings. Condor 71: 41g-425, 1%9. 132. Southern, W. E. Gull orientation by magnetic cues: A hypothesis revisited. Ann. N.Y. Acad. Sci. 188: 295-311, 1971. 133. Southern, W. E. Influence of disturbances in the earth's magnetic field on Ring-billed gull orientation. Condor 74: 102-105, 1972. 134. Southern, W. E. Magnets disrupt the orientation of juvenile Ring-billed gulls. Bioscience 22: 476-479, 1972. 135. Southern, W. E. Effects of simulated and natural magnetic disturbances on avian orientation. Wilson Bull. 86: 256-271, 1974. 136. Southern, W. E. Orientation of gull chicks exposed to Project Sanguine's electromagnetic field. Science 189: 143-145, 1975. 137. Stewart, O. J. A bird's inborn navigational device. Trans. Kent. Acad. Sci. lg: 78-84, 1957. 138. Stutz, A. M. Effects of weak magnetic fields on gerbil spontaneous activity. Ann. N.Y. Acad. Sci. 188: 312-323, 1971. 139. Talkington, L. Bird navigation and geomagnetism. Am. Zool. 4: 199, 1964. 140. Talkington, L. On Bird Navigation. Paper presented at the 131st annual Meeting of the American Association for the Advancement of Science. Montreal, December, 1964. 141. Talkington, L, and L. C. Graue. Exploratory Work on Bird Navigation. Interim report to National Science Foundation, Report No. GB-5239, 1%7. 142. Tanner, J. A. and C. Romero-Sierra. Bird feathers as sensory detectors of microwave fields. In: Symposium on the Biological Effects and Health Implications o f Microwave Radiation, edited by S. F. Cleary. Bureau of Radiological Health, Report No. BRH/DBE 70-2, Virginia Commonwealth University, September, 1969. (NTIS No. PB 193 898.) 143. Tanner, J. A., C. Romero-Sierra and S. T. Davie. Non-thermal effects of microwave radiation in birds. Nature, Lond. 216: 1139, 1967. 144. Tasaki, I. and J. J. Chang. Electric responses of glia cells in cat brain. Science 128: 1209-1210, 1958. 145. Travkin, M. P. Effect of a weak magnetic field on the bioelectric potentials of Tradescantia. Fiziol. Rast. 19: 448--450, 1972.

269

146. Tshernyshev, W. B. and M. L. Danilevsky, The effect of the alternative magnetic field on the activity of flies Protophormia terrae-novae R.D.. Zh. Obsch. Biol. 27: 4%-498, 1966. 147. Varian, R. H. Remarks on: " A preliminary study of a physical basis of bird navigation." J. appl. Physiol. 19: 306-307, 1948. 148. Wagner, G. Das Orientierungsverhalten von Brieftauben im erdmagnetisch gestrrten Gebiete des Chasseral. Rev. suisse Zool. 83: 883-890, 1976. 149. Walcott, C. Bird navigation. Nat. Hist. N.Y. 81(6): 32-42, 1972. 150. Walcott, C. The navigation of homing pigeons: Do they use sun navigation? In: Animal Orientation and Navigation, edited by S. R. Galler, K. Schmidt-Koenig, G. J. Jacobs and R. E. Belleville. Washington, D.C.: U.S. Government Printing Office, 1972, pp. 283-292. (NASA SP-262). 151. Walcott, C. Magnetic fields and the orientation of homing pigeons under sun. J. exp. Biol. 70: 105-123, 1977. 152. Walcott, C. and R. P. Greene. Orientation of homing pigeons altered by a change in the direction of an applied magnetic field. Science 184: 180-182, 1974. 153. Wallraff, H. G. Versucbe zur Frage der gerichteten Nachtzug-Aktivit/it von gek51]gten Singvrgeln. Verh. dt. zool. Ges. Jena, 1965, 1%5, pp. 339-356. 154. Wehner, R. and T. Labhart. Perception of the geomagnetic field in the fly, Drosophila melanogaster. Experientia 26: 967968, 1970. 155. Werber, M., R. M. Sparks and A. C. Goetz. The behavior of weakly electric fish (Sternarchus albifrons) in magnetic fields. J. genet. Psychol. 86: 3-13, 1972. 156. Wiltschko, W. Uber den Einfluss statischer Magnetfelder auf die Zugorientierung der Rotkehlchen (Erithacus rubecula). Z Tierpsychol. 25: 537-558, 1%8. 157. Wiltschko, W. The influence of magnetic total intensity and inclination on directions preferred by migrating European robins (Erithacus rubecula). In: Animal Orientation and Navigation, edited by S. R. Galler, K. Schmidt-Koenig, G. J. Jacobs and R. E. Belleville. Washington, D.C.: U.S. Government Printing Office, 1972, pp. 569-578. (NASA SP-262). 158. Wiltschko, W. Evidence for an innate magnetic compass in garden warbles. Naturwissenschaften. 61: 406, 1974. 159. Wiltschko, W. Der Magnetkompass der Gartengrasmiicke (Sylvia borin). J. Orn. 115: 1-7, 1974. 160. Wiltschko, W., H. Hrck and F. W. Merkel. Outdoor experiments with migrating European robins in artificial magnetic fields. Z. Tierpsychol. 29: 409-415, 1971. 161. Wiitschko, W. and F. W. Merkel. Orientierung zugunruhiger Rotkehlchen im statischen Maguetfeld. Verh. dr. zool. Ges. Jena, 1965, 1965, pp. 362-367. 162. Wiltschko, W. and F. W. Merkel. Zugorientierung von Dorngrasmiicken (Sylvia communis) im Erdmagnetfeld. Vogelwarte 26: 245-249, 1971. 163. Wiltschko, W. and R. Wiltschko. Magnetic compass of European robins. Science 176: 62-64, 1972. 164. Wiltschko, W. and R. Wiltschko. The interaction of stars and magnetic field in the orientation system of night migrating birds. I. Autumn experiments with European warbler (Gen. Sylvia). Z. Tierpsychol. 37: 337-355, 1975. 165. Wiltschko, W. and R. Wiltschko. The interaction of stars and magnetic field in the orientation system of night migrating birds. II. Spring experiments with European robins (Erithacus rubecula). Z. Tierpsychol. 39: 265-282,1975, 166. Wiltschko, W. and R. Wiltschko. Die Bedeutung des Magnetkompasses fOr die Orientierung der VOgel. J. Orn. 117: 362387, 1976. 167. Wiltschko, W. and R. Wiltschko. Interrelation of magnetic compass and star orientation in night-migrating birds. J. comp. Physiol. 109: 91-99, 1976. 168. Wodzicki, K,, W. Puchalski and H. Liche. Untersuchungen fiber die Orientation and Geschwindigkeit des Fluges bei VOgeln. V. Weitere Versuche an Strrchen. J. Orn. 87: 99-114, 1939.

270 169. Wojtusiak, R. J. Orientation in birds. Przeglad Zoologic.'.ny 4: 254-271, 1960. 170. Yakovleva, M. I. and M. V. Medvedeva. Conditioned control of cardiac activity and respiration and morphological changes in the brain of pigeons under the effect of a constant magnetic field. Zh. vyssh, nerv. Deyat. I.P. Pavlova 22: 288-293, 1972. (NTIS No. AD-784 798).

OSSENKOPP AND BARBEIT() 171. Yeagley, H. L. A preliminary study of a physical basis of bird navigation. J. appl. Physiol. 18: 1035-1063, 1947.