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Animal navigation: How animals use environmental factors to find their way
Migratory animals have innate programs to guide them to their still unknown goal. Highly mobile animals with large ranges develop a so-called navigational ‘map’, a mental representation of the spatial distribution of navigational factors within their home region and their migration route. We present here the first part of the paper. The concluding part will be published in December issue |
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Abstract
Animals use the geomagnetic field and astronomical cues to obtain compass information. The magnetic compass is not a uniform mechanism, as several functional modes have been described in different animal groups. The Sun compass requires the internal clock to interpret the position of the Sun. For star compass orientation, night migrating birds seem to use the star pattern as a whole, without involving the internal clock. Both the astronomical compass mechanisms are based on learning processes to adapt them to the geographic latitude where the animals live and, in long living animals, to compensate for the seasonal changes. Several mechanisms are used to determine the compass course to a goal. Using information collected during the outward journey is mostly done by path integration: recording the direction with a compass and integrating its twists and turns. Migratory animals have innate programs to guide them to their still unknown goal. Highly mobile animals with large ranges develop a so-called navigational ‘map’, a mental representation of the spatial distribution of navigational factors within their home region and their migration route. The nature of the factors involved is not yet entirely clear; magnetic intensity and inclination are the ones best supported so far.
1 Introduction
Many animals perform extended migrations. Most famous are the annual migrations of millions of birds that, in autumn, leave regions with adverse winter conditions to overwinter in more favorable parts of the Earth. The record holder in distance is the Arctic tern, Sterna paradisea, a sea bird breeding in the Arctic regions that spends the winters at the edge of the Antarctic Continent, thus staying in eternal summer, avoiding coldness and darkness. But many other birds migrate as well, covering several thousand kilometers every year; among them are, e.g., water birds, raptors, swifts and small songbirds such as swallows, warbler and others. They spend the summer in the northern temperate zones and move to lower latitudes, some of them crossing the equator for wintering. Whales cover long distances between their Arctic or Antarctic feeding grounds and areas with warmer water where they give birth to their calves. But also terrestrial mammals, like many hoofed animals, perform long distance migrations to follow the annual change in vegetation, e.g., the caribous in northern Canada or zebras, gnus and antelopes in eastern Africa. Some animals migrate between nesting and feeding grounds, e.g., marine turtles. Many fishes migrate; some of them, like eels and salmons, only at the beginning and end of their life. Even some insects migrate: the monarch butterfly, Danaus plexipus, is a prominent example.
Most of these migrations involve specific routes and defined end points. Eels and salmons, as well as marine turtles are known to leave their feeding sites after years to return to the places where they were born to lay their eggs. Banded birds were found to return to the same breeding site year after year, and many of them seem to spend the non-breeding season in the same wintering grounds every year.
Birds are also known to return after passive displacement from unfamiliar sites. Homing pigeons, Columba livia domestica, bred from the Mediterranean rock dove, were domesticated and used to transport messages already since antiquity. But other bird species, too, were found to be able to compensate for displacements; that is, they can directly head toward a specific goal. The same appears to be true for numerous other animals, with the distances involved correlated with the size of their home range.
Yet, the ability to navigate is not only required for extended migrations and displacements like those mentioned above, but also during their everyday movements within their home range animals profit greatly from good orientation, because it is advantageous to optimize routes—this saves energy and helps to avoid predation.
To answer the question what factors animals use to navigate, it is important to understand how they proceed when they want to reach a specific goal. Birds are by far the best studied group— homing pigeons are available ad libitum and can be easily used for orientation experiments. When they are released at a distant site, they leave this site heading in directions close to the home direction. With migratory birds, their innate tendency to seasonally move in their migratory directions provides a reliable, solid baseline for cage experiments. Hence much of our present knowledge on animal navigation comes from studies with birds, but many of the processes and procedures identified in birds seem to have parallels in other animals.
2 The “Map-andCompass” model
Systematic research on animal navigation began in the second half of the twentieth century, when Gustav Kramer [1] and Karl von Frisch [2] in 1950 reported that birds and bees can use the Sun for orientation. The Sun compass, thus, was the first orientation mechanism described (see below). In the course of his experiments with homing pigeons, Kramer recognized that avian navigation is a two step process and proposed his Map-and-Compass model (e.g., [3]): When birds intend to return home from a distant site, they first determine the compass course leading to the goal and then use a compass to look up this direction and follow it home. Thus the first step of navigation, the Map step means applying mechanisms for determining the present position and put it in directional relation to the goal, and the second step, the Compass step, means applying mechanisms which allow to locate specific directions.
The Map-and-Compass model was first developed to describe the homing process of pigeons after displacement, with the Sun compass for the compass step, while the mechanisms by which the pigeons determine their home course could not yet be identified. This model, however, can be expanded to characterize avian navigation in general. In the beginning, young birds use information obtained during the outward journey, and for the first migration to the still unknown wintering area, the map step is replaced by a genetic program that makes birds move into an innate direction for a certain time. Experienced birds, however, are then able to truly navigate, using local site specific information, within and beyond their home region as well as during migration (for review, see, e.g., [4]). Little is known about the navigation procedures of other animals, but we tend to assume that in many cases they might proceed in a similar way when they have to reach a specific goal. However, in some cases under certain conditions, they might use more direct mechanisms.
When Kramer [3] proclaimed the Mapand-Compass model, the Sun compass was the only navigational mechanism yet known. Research during the last decades increased our knowledge on the factors and mechanisms of animal navigation considerably, even if many questions are still open. In particular, the compass mechanisms have fairly well been analyzed in many animals.
3 Compass mechanisms
How do animals proceed when they have to locate directions? In principle, they use the same factors that we humans, too, use, namely the geomagnetic field and astronomical cues. Three compass mechanisms have been identified in animals, namely a magnetic compass, a Sun compass for directional orientation during the day and a star compass for orientation at night.
3.1 The magnetic compass
We humans need a technical device—a compass where a magnetic needle aligns itself with the course of the field lines— to locate the direction of the geomagnetic field. Many animals, in contrast, can sense the direction of the magnetic field directly.
3.1.1 The distribution of a magnetic compass among animals
A sense for magnetic directions was first discovered in migratory birds: During the migratory season, these birds show a spontaneous tendency to prefer their migratory direction also in suitable cages, and when the north of the ambient magnetic field was shifted by a coil system, European robins (Erithacus rubecula, Turdidae) changed their preferred direction accordingly (Fig. 1a, b) [5]. These findings initially met with considerable skepticism because it was a novel, unexpected sensory ability alien to man. Meanwhile, however, a magnetic compass has been demonstrated in more than 20 bird species, including other migrants and also in non-migrants, e.g., homing pigeons [6] and even domestic chicken (Gallus gallus domesticus)[7]. It was also found in animals of other groups, first in cave salamanders [8], but soon also in all groups of vertebrates— in fish such as stingrays [9], salmons [10,11], eels [12,13] and others, in frogs (e.g., [14]), alligators [15], marine turtles [16] and mammals like rodents [17] and bats [18]. Findings in humans have been controversially discussed (see [19]).
A magnetic compass was also demonstrated in sea slugs (Nudibranchia) [20], in crustaceans like spiny lobsters [21], sandhoppers (Amphipoda) (e.g., [22]) and others, and also in insects such as termites [23], beetles [24], moths [25] and butterflies (e.g., [26]), honeybees [27] and ants [28,29]. A magnetic compass thus appears to be widespread and may even be a general characteristic of mobile animals.
3.1.2 Different functional modes
The magnetic compass in animals is not a uniform mechanism, however. It has been analyzed in detail only in very few species so far, but there are at least two fundamentally different functional modes and some modifications. The mechanisms in birds are the ones best known so far and, here, the magnetic compass functions very differently from our technical compass.
Birds are not sensitive to the polarity of the magnetic field (see Fig. 1a, c); instead, they sense the axial course of the field lines and distinguish between their two ends by the inclination [30]. This means that for birds, the magnetic compass does not indicate magnetic north and south, as our technical compass does, but poleward, where the field lines point downward and equatorward, where they point upward. This type of compass, an inclination compass, becomes ambiguous at the magnetic equator and requires long distance migrants to ‘reverse’ their heading from equatorward to poleward when they cross the equator to continue heading southward. The inclination compass was first analyzed in European robins, but was also found in all other bird species tested for it so far. It is remarkably accurate; it was shown to still work at an inclination of 87◦, i.e., only 3◦from the vertical [31,32] and at 5◦, close to the horizontal [33].
The avian magnetic compass proved to be light dependent, requiring short wavelength light from UV to about 565 nm green (see Fig. 1); under red light, birds are disoriented [34–36]. It spontaneously functions only in magnetic intensities with which the birds are familiar; decreasing or increasing the ambient intensity about 25% leads to disorientation [37,38]. However, birds can adjust to intensities outside this functional window when they are exposed to other intensities for a while: Robins caught and kept in a field of 46 µT thus became able to orient at intensities as low as 5 nT [39] and as high as 150 nT, but could not orient at the intermediate intensity of 81 nT [37]. This ability allows migrating birds to cope with the decreasing intensities that they encounter when reaching lower latitudes.
These characteristics of their magnetic compass indicate that birds have a specific way to perceive magnetic directions. In the 1980s, Schulten and Windemuth [40] suggested the radical pair model, which was later detailed by Ritz and colleagues. It assumes the avian magnetic compass to be based on radical pair processes, with the direction of the ambient magnetic field changing the ratio singlet/triplet of the radical pair (for details, see [41]). This effect does not depend on the polarity of the magnetic field and thus results in an inclination compass as found in birds.
As site of magnetoreception, the authors suggested the eyes, because of their spherical shape, and there are receptor cells aligned in all spatial directions. Hence the different ratio of singlet/triplet would result in an activation pattern on the retina that is centrally symmetric to the course of the field lines (see [41] for details). Changes in intensity would modify the activation pattern, which appears to confuse the birds at first, but since the pattern retains its central symmetry to the field lines, birds can learn to interpret the altered pattern.
As receptor molecule providing the radical pairs, Ritz and colleagues suggested cryptochrome, a protein with FAD (flavin adenine dinucleotide) as chromophore [41], because it is the only known photo pigment in animals that forms radical pairs. Several types of cryptochromes were indeed found in the retina of birds (see, e.g., [42]). In particular Cry1a, located in the outer segment of the V/UV receptor cells of robins, chickens and zebra finches (Taeniopygia guttata, Estrldidae) seems highly suitable for magnetoreception. These cells are distributed all across the retina [43,44] and thus could produce the assumed activation pattern. Cry1a is activated at all wavelengths where birds were found to be oriented [45]. Later studies indicate that the crucial radical pair is formed during reoxidation ([46]; for review, see [42]).
Amphibians and marine turtles were also shown to have an inclination compass, i.e., a compass that is not sensitive to the polarity of the magnetic field. Their compass mechanisms, however, were found to differ from that of birds in their light dependency. While birds are still oriented under 565 nm green light, the wave length range of normal orientation in the newt Nothophthamus (Salamandridae) appears to end at about 450 nm blue [47]. Marine turtles, in contrast, could use their inclination compass also in total darkness [48]. Only little is known about the magnetic compass of other vertebrates .A few fishes and mammals have been studied: salmons [49], subterranean rodents [50], and bats [51] were found to respond to the polarity of the magnetic field—they have a polarity compass. Details of their reception mechanisms have not yet been analyzed; permanent magnetic material like magnetite (a specific form of iron oxide, Fe(II)Fe(III)2O4) has been discussed.
Even less is known about the functional mode of the magnetic compass of arthropods. Among crustaceans, only the compass mechanism of spiny lobsters has been analyzed; they were found to have a polarity compass [52]. The two species of insects tested so far, the flour beetle Tenebrio [53] and the monarch butterfly [54], in contrast, have an inclination compass.
The different functional modes of the magnetic compass suggest independent evolutionary developments. The magnetic compass is an important orientation mechanism with the great advantage of being always available, independent of the time of the day and the weather conditions. Magnetic disturbances, such as magnetic storms and local anomalies, are rarely strong enough to interfere with it.
3.2 The Sun compass
The Sun is widely used for direction finding during the day. The first indications of the Sun as an orienting cue were already reported in the beginning of the twentieth century, when Santschi [55] could redirect ants by reflecting the Sun with a mirror. In 1950, the Sun compass was discovered independently in animals as different as birds [1], and in honeybees [2]. This initiated a systematic search for Sun compass orientation in the animal kingdom. Soon a Sun compass was found in various crustaceans (summarized by [56]), various insect groups like ants and bees, beetles and others, spiders (summarized by [57,58]), butterflies like the Monarch [59], and marine snails [60]. Among vertebrates, it was found in several species of fishes (e.g.,[61]; for review see [62]), in reptilian species such as lizards [63], snakes [64,65], turtles [66,67] and alligators [68]). Yet in amphibians (e.g., [69]) and mammals, where rodent species were tested (e.g., [70]), the data were less clear. It has to be considered, however, that amphibians mostly avoid being exposed to clear sunlight, and rodents are mostly nocturnally active.
3.2.1 Functional mode and ontogeny of Sun compass orientation
To derive directional information from the Sun, the animals must know the Sun’s arc and consider the time of the day. This does not pose a problem, because animals are endowed with an internal clock. Their endogenous circadian rhythm is synchronized with the natural day by sunrise and sunset, (see, e.g., [71]). With this sense for the time of the day, they interpret the Sun’s position. The customary demonstration of Sun compass use is based on this phenomenon. In the socalled clock-shift experiments, the internal clock of the test animals is shifted, mostly for 6 h, by subjecting them to an artificial photoperiod that, e.g., starts 6 h before sun-rise and ends 6 h before sunset. After about 5 days, the internal clock is adjusted to the new, artificial photoperiod. When the animals are then exposed to the Sun, they misjudge its position and orient in a direction that deviates markedly from that of untreated controls—in the Northern Hemisphere, a forward shift results in a counterclockwise, and a backward shift in a clockwise deviation (Fig. 2). Such clockshift experiments were first conducted by Schmidt Koenig [71] with homing pigeons, but soon this method has been widely applied, e.g., also in connection with directional training (see e.g., [72])
When animals are tested in a clock-shift experiment, the altitude of the Sun is markedly different from what they should expect according to their subjective time, e.g., 6 h forward shifted pigeons tested at 6:00 in the morning should expect the Sun high up in the sky because this is their subjective noon; instead it is low above the horizon. They seem to ignore this discrepancy, however, which indicates that for the Sun compass of birds, only the Sun’s azimuth is important, whereas its altitude is ignored. Schmidt–Koenig therefore describe the Sun compass of pigeons as a Sunazimuth compass ([72]; see also, e.g., [73] for ants). The same seems to apply to many other animals; for fishes, however, the Sun’s altitude seemed to be also involved in the orientation process (see e.g., [74]).
Yet the Sun’s azimuth does not change uniformly in the course of the day; just after sunrise and just before sunset, when the Sun rapidly gains or loses altitude, its increase is rather slow, below the average of 15◦per hour, whereas around noon, when the Sun is high up in the sky, it moves much faster. This raised the question whether the animals are aware of this and compensate for the changes in azimuth correctly. This was first demonstrated in the desert ant Cataglyphis (Formicidae): These ants are aware of the different rates of change in the course of the day [73] and interpret the Sun’s azimuth accordingly. The same appears to apply to honeybees [75,76]. Fishes, too, consider the different rates of change in Sun’s azimuth largely correctly [77], and this is also true for birds [78].
The Sun’s arc, however, and with it the rate of changes in azimuth, depends on the geographic latitude and season. This means that for precise Sun compass orientation, the animals’ compensation mechanisms must be based on the true Sun’s arc of their home region and the correct time of the year. This is accomplished by learning processes: ants and bees observe the sky before they begin the foraging phase of their life. These learning processes are rather fast, taking only a few days, and seem to be supported by innate components (see e.g., [79] for details)—ants that had experienced the Sun only early in the morning could interpret its position in the afternoon correctly [80]. This is probably required because of the rather short life span of these social insects, which also makes an adaptation to the seasonal changes largely unnecessary. Ants that have overwintered, however, must learn the Sun compass in spring anew [81], which may also apply to over wintering bees.
In birds, the ontogeny of the Sun compass has been studied only in homing pigeons. Here, it is likewise learned [82], with the learning processes taking considerably longer and requiring observation of the Sun’s arc during large portions of the day. Birds that had experienced the Sun only in the afternoon could not use their Sun compass in the morning [83]. Learning the Sun compass normally begins when the pigeons are about 12 weeks old, but it can be advanced by early flying experience [84]. The magnetic compass serves as reference against which the movement of the Sun is observed [85]. We tend to assume that the respective processes are similar in all bird species. How the avian Sun compass is adjusted to the seasonal changes has not yet been analyzed; it is to be expected, however, that the processes are similar to those of its first establishment. Little is known about the establishment of the Sun compass in other animals. Experiments with fishes that never saw the natural Sun suggested that their Sun compass may be in large parts innate (see [85]).
The Sun compass is the most important orientation mechanism within the animals’ home range and over shorter distances, where animals follow their Sun compass in spite of contradicting information from their magnetic compass. During long range migrations, however, animals would have to additionally cope with the changes of the Sun’s arc with geographic latitude or, when they migrate east/west, with the resulting shift in local time. Interestingly, while a Sun compass was demonstrated in numerous fish species (see e.g.,[60,61], experiments involving migration with species like salmons and eels failed to produce unequivocal evidence for Sun compass orientation [87,88]. With birds, the Sun compass is likewise demonstrated in displacements and conditioning (see e.g., [89] for summary), but day migrating birds during migration did not respond to clock shifting as expected (e.g., [90]). The findings suggested that they paid attention to the Sun, but that the Sun compass does not serve as major compass system for orienting the migration flight.
3.2.2 The role of polarized light
The Sun is accompanied by a particular pattern of polarization in the sky light, with the polarization reaching a maximum 90◦from the Sun. It gradually changes as the Sun moves. In contrast to us, many animals can see this polarization pattern in the sky and use it for orientation, so that for them, the Sun compass is actually a ‘skylight’ compass (see e.g., [91]). The pattern of polarization is also visible below the water surface (see e.g., [92]) so that polarized light is also a potential orientation cue for aquatic animals living near the surface. Responses to polarized light have indeed been observed in crustaceans such as Daphnia (e.g.,[93]) and decapods [94].
The use of polarized light for orientation was first discovered in honeybees and ants [95,96] and in the following years was also found in many other insect species. In insects, where the upper parts of the eyes are specialized to detect the polarization of light (for reviews, see e.g., [57,97]; for details about the insects’ polarization vision, see e.g., [98]). Experiments with desert ants of the genus Cataglyphis showed that these ants are familiar with the polarization pattern and its changes in the course of the day; they use it for compass orientation [80]. They need not see the entire sky, but a small portion is suffcient. Dung beetles have even been reported to be able to use the polarized moonlight for nocturnal orientation [99].
Many vertebrates, too, are sensitive to polarized light. This is indicated in fishes (e.g., [100]), amphibians [101], reptiles (e.g., [102,103]) and, among mammals, bats [104]. Birds are also able to perceive polarized light [105] and with them the effect of polarized light on orientation behavior has been studied in some detail. The pattern of polarized light at sunset was shown to play some role in the orientation of a night migrating American songbird [106] that starts migra-tion flight at about that time. Several authors began to test the relative importance of polarized light compared to other cues, with some studies appearing to indicate a dominance of polarized light [107– 109]. Several of these studies are not unproblematic, however, because they involved polarizers, which polarize the entire skylight almost 100%, and this unnatural pattern appears to alter the normal behavior. Birds were observed to orient roughly parallel to the axis of polarization, which was significantly different from their response to the natural polarization pattern [110]. A dominant role of polarization could not be generally confirmed (e.g., [111,112] a.o.).
Yet migratory birds can use the natural polarization pattern for orientation. A twilight migrant stayed oriented when other orienting cues like the geomagnetic field had been removed (e.g., [113]), and this is also applicable for a day migrant. In a compensated magnetic field, the birds were still oriented as long as the natural skylight was visible, even when the Sun itself was obscured [114].
A crucial role of polarized light is also that it can mediate celestial rotation to migratory birds, which is an important factor for transforming the genetically coded information on the migratory direction into an actual direction (see below). This effect was only observed in birds that had full view of the natural sky, whereas birds that had observed the sky through depolarizers could not do so, even if they had been able to see the Sun and its movement [115].
The Sun compass, i.e., the skylight compass, is the dominant mechanism in the compass orientation of many animals: They prefer to use it when it is available.
3.3 The star compass
Using the stars for orientation has been described so far only for nocturnally migrating birds; they can use the stars as a compass. This was first demonstrated in planetarium experiments. Reversing the planetarium sky caused birds to reverse their headings (Fig. 3) [116,117].
A star compass is also indicated by outdoor experiments, where birds at night headed in their migratory direction with the stars as only available cue (e.g., [118–120]).
The stars move in the course of the night, but an analysis of the star compass showed that the internal clock was not involved [121]. This excluded mechanisms similar to that of the Sun compass (see above) and spoke against the use of individual stars, suggesting that birds might derive directions from the pattern as a whole or parts of the pattern. Experiments blocking certain constellations revealed a considerable individual variance. In general, the circumpolar stars within 35◦of the center of rotation center seemed to be important, yet the results did not allow a final conclusion [121].
The star compass is also a learned mechanism. Young migrants could use the stars as a compass only if they had observed the sky rotating before they start autumn migration. In an experiment, two groups of hand raised birds were exposed to a rotating planetarium sky, with the control group under the normal sky, rotating around the polar star Polaris, while the test group was exposed under a sky rotating around Betelgeuze in Orion. Later, during autumn migration, both groups were tested under the now stationary planetarium. The control group preferred the normal southerly migratory direction, heading away from Polaris, whereas the test group headed away from Betelgeuze [122]. Birds do not seem to have an innate concept about what the sky looks like. The complex natural sky could be replaced by a simple pattern of only 16 light dots—as long as the birds had observed this pattern rotating with 1 rotation per day, they later could use it to orient in their migratory direction relative to the center of rotation [123,124]. Celestial rotation was thus identified as the crucial factor for establishing the migratory direction with respect to the stars.
The view of the sky changes gradually. The stars rise 4 min earlier each day, so that the sky in autumn looks different from that in spring. At the same time, the sky changes its appearance with geographic latitude. During autumn migration, as the bird moves south, the northern stars slowly lose altitude and approach the horizon, while new stars appear at the southern horizon. Birds have to integrate these new stars into their star compass. Experiments under the natural sky with altered magnetic fields indicate that the magnetic compass provides the reference system which gives directional meaning to the new stars during migration (e.g.,[118,119], a.o.).
So far, a star compass has been demonstrated only in a few species of songbirds that migrate at night. Since the majority of birds are primarily day active, the star compass could be a special mechanism developed by the nocturnal migrants to orient their extended flights. It is unknown whether generally night active birds, like, e.g., nightjars or owls, also use the stars as a compass as such birds have not yet been studied.
References
1. G. Kramer, Naturwissenschaften 37, 377 (1950)
2. K.V. Frisch, Experientia 6, 210 (1950)
3. G. Kramer, Ibis 101, 196 (1959)
4. R. Wiltschko, W. Wiltschko, Adv. Study Behav. 47, 229 (2015)
5. W. Wiltschko, W. Z. Tierpsychol. 25, 536 (1968)
6. W.T. Keeton, Proc. Natl. Acad. Sci. USA 68, 102 (1971)
7. R. Freire, U.H. Munro, L.J. Rogers, R. Wiltschko, W. Wiltschko, Curr. Biol. 15, R620 (2005)
8. J.B. Phillips, J. Comp. Physiol. 121, 273 (1977)
9. A.J. Kalmijn, in Sensory Biology of Sharks, Skates, and Rays edited by F.S. Hodson, R.F. Matthewson (Office Naval Res., Arlington, VA 1978), p. 307
10. T.P. Quinn, J. Comp. Physiol. 137, 243 (1980)
11. P.B. Taylor, J. Fish. Biol. 28, 607 (1986)
12. J. Karlsson, Helgol. Meeresunters. 39, 71 (1985)
13. J.J. Souza, J.J. Puluhowich, R.J. Guerra, Comp. Biochem. Physiol. 90A, 57 (1988)
14. T. Leucht, J. Exp. Biol. 148, 325 (1990)
15. G.H. Rodda, J. Comp. Physiol. A 154, 549 (1984)
16. K.J. Lohmann, J. Exp. Biol. 155, 37 (1991)
17. H. Burda, S. Marhold, T. Westenberger, R. Wiltschko, W. Wiltschko, Experiencia 46, 528 (1990)
18. R.A. Holland, K. Thorup, M.J. Vonhof, W.W. Cochan, Nature 444, 702 (2006)
19. R.R. Baker, Anim. Behav. 35, 691 (1987)
20. K.J. Lohmann, A.O.D. Willows, Encyclopedia of Neuroscience (Birkh¨auser, Boston, 1987), p. 331. (Suppl. 1)
21. K.J. Lohmann, Mar. Behav. Physiol. 12, 1 (1985)
22. L. Pardi, A. Ercolini, F. Ferrara, F. Scapini, Atti Accad Lincei Rend. Sci. Fis. Mat. Nat. 75, 312 (1985)
23. M. Rickli, R.H. Leuthold, Ethology 77, 209 (1988)
24. M.C. Arendse, J.C.M. Vrins, Neth. J. Zool 25, 407 (1975)
25. R.R. Baker, J.G. Mather, Anim. Behav. 30, 343 (1982)
26. J.A. Etheredge, S.M. Perez, O.R. Taylor, R. Jander, Proc. Natl. Acad. Sci. USA 96, 13845 (1999)
27. D. DeJong, J. Comp. Physiol. 147, 493 (1982)
28. R. Jander, U. Jander, Ethology 104, 743 (1988)
29. P.N. Fleischmann, B. Grob, V.I. M¨uller, R. Wehner, W. R¨ossler, W. Curr. Biol. 28, 1440 (2018)
30. W. Wiltschko, R. Wiltschko, Science 176, 62 (1972)
31. S. ˚Akesson, J. Morin, R. Muheim, U. Ottoson, U. Pole, Proc. R. Soc. Lond. B 268, 19097–1913 (2001)
32. N. Lefeldt, D. Dreyer, N.-L. Scheider, F. Steenken, H. Mouritsen, J. Exp. Biol. 218, 206 (2015)
33. S. Schwarze, F. Steenken, N. Thiele, D. Kolbykov, N. Lefeldt, D. Dreyer, N.-S. Schneider, H. Mouritsen, Sci. Rep. 6, 33805 (2016)
34. W. Wiltschko, R. Wiltschko, Nature 364, 525 (1993)
35. W. Wiltschko, R. Wiltschko, J. Comp. Physiol. A 177, 363 (1995)
36. R. Muheim, J. B¨ackman, S. ˚Akesson, J. Exp. Biol. 205, 3845 (2002)
37. W. Wiltschko, in Animal Migration, Navigation, and Homing edited by K. Schmidt-Koenig, W.T. Keeton (Springer, Berlin, 1978), p. 302
38. W. Wiltschko, R. Freire, U. Munro, T. Ritz, L. Rogers, P. Thalau, R. Wiltschko, J. Exp. Biol. 210, 2300 (2007)
39. M. Winklhofer, E. Dylda, P. Thalau, W. Wiltschko, R. Wiltschko, Proc. R. Soc. Lond. B. 280, 20130850 (2013)
40. K. Schulten, A. Windemuth in Biophysical Effects of Steady Magnetic Fields edited by G. Maret, N. Boc-cara, J. Kiepenheuer (Springer, Berlin, 1986) p. 99
41. T. Ritz, S.Adem, K. Schulten, Biophys. J. 78, 797 (2000)
42. R. Wiltschko, W. Wiltschko, Front. Physiol. 12, 667000 (2021)
43. C. Nießner, S. Denzau, J.C. Gross, L. Peichl, H.- J. Bischof, G. Fleissner, W. Wiltschko, R. Wiltschko, PloS One 6, e20091 (2011)
44. A. Pinzon-Rodriguez, R. Muheim, Sci. Rep. 11, 12683 (2021)
45. C. Nießner, S. Denzau, K. Stapput, M. Ahmad, L. Peichl, W. Wiltschko, R. Wiltschko, J.R. Soc, Inter-face 10, 20130630 (2013)
46. R. Wiltschko, M. Ahmad, C. Nießner, D. Gehring, W.Wiltschko, R. Wiltschko, J.R. Soc, Interface 13, 20151010 (2016)
47. J.B. Phillips, S.C. Borland, Ethol. Ecol. Evol. 4,33 (1992)
48. K.J. Lohmann, C.M.F. Lohnmann, Biol. Bull. 185, 149 (1993)
49. T.P. Quinn, R.T. Merrill, E.L. Brannon, J. Exp. Biol. 21, 137 (1981)
50. P. Thalau, T. Ritz, H. Burda, R.E. Wegner, R.E. Wiltschko, J. R. Soc. Interface 3, 583 (2006)
51. Y. Wang, Y. Pan, S. Parsons, M. Walker, S. Zhang, Proc. R. Soc. Lond. B 274, 2901 (2007)
52. K. Lohmann, N.D. Pentcheff, G.A. Nevitt, G.D. Stet-ten, R.K. ZimmerFaust, H.E. Jarrard, L.C. Boles, J. Exp. Biol. 198, 2041 (1995)
53. M. V´acha, D. Drˇstkov´a, T. P˚uˇzova, Naturwissenschaften 95, (2008)
54. P.A. Guerra, R.J. Gegear, S.M. Reppert, Nat. Commun. 5, 4164 (2014)
55. F. Santschi, Revue Suisse de Zoologie 19, 303 (1911)
56. L. Pardi, Cold Spring Harbour Sym. Quant. Biol. 25, 395 (1960)
57. K. von Frisch, Tanzsprache und Orientierung der Bienen (Springer, Berlin, 1965)
58. K. Schmidt-Koenig, Migration and Homing in Ani-mals, Zoophysiology and Ecology 6 (Springer, Berlin, 1975)
59. S.M. Perez, O.R. Taylor, R. Jander, Nature 387,29 (1997)
60. K. Warburton, Mar. Biol. 23, 93 (1973)
61. A. Hasler, R.M. Horral, W.J. Wisby, W. Braemer, Lim-nol. Oceanogr. 3, 353 (1958)
62. T. Waterman, in Animal Orientation and Navigation edited by S.R. Galler, K. Schmidt-Koenig, G.J. Jacobs, R.E-Belleville (NASA SP-262, Washington, D. C., 1972), p. 437
63. K. Fischer, Naturwissenschaften 47, 287 (1960)
64. R.T. Newcomer, D.H. Taylor, S.L. Guttman, Herpetologia 30, 194 (1974)
65. J.S. Robinson, G.G. Murphy, J. Tenn. Acad. Sci. 51, 59 (1976)
66. K. Fischer, Verh. Dtsch. Zool. Ges. 1965, 546 (1965)
67. C.T. DeRosa, D.H. Taylor, Am. Zool. 16, 245 (1976)
68. P.A. Murphy, Copeia 3, 638 (1981)
69. D.E. Ferguson, Ann. N. Y. Acad. Sci. 188, 30 (1971)
70. S.L. Fluharty, D.H. Taylor, G.W. Barrett, J. Mammal. 57, 1 (1976)
71. J. Aschoff, Naturwissenschaften 41, 49 (1954)
72. K. Schmidt-Koenig, Z. Tierpsychol. 18, 221 (1961)
73. R. Wehner, B. Lanfranconi, Nature 293, 731 (1981)
74. W. Braemer, Cold Spring Harbour Sym. Quant. Biol. 25, 413 (1960)
75. D.A.T. New, J.K. New, J. Exp. Biol. 39, 363 (1962)
76. F.C. Dyer, J.A. Dickinnson, Proc. Natl. Acad. Sci. USA 91, 4471 (1994)
77. H.O. Schwassmann, W. Braemer, Physiol. Zool. 34, 273 (1961)
78. R. Wiltschko, M. Walker, W. Wiltschko, J. Exp. Biol. 203, 889 (2000)
79. M. Lindauer, Z. Vergl, Physiol. 42, 43 (1959)
80. R. Wehner, M. M¨uller, Naturwissenschaften 80, 331 (1993)
81. R. Jander, Z. Vergl. Physiol. 40, 162 (1957)
82. W. Wiltschko, R. Wiltschko, W.T. Keeton, Behav. Ecol. Sociobiol. 1, 229 (1976)
83. R. Wiltschko, D. Nohr, W. Wiltschko, Science 214, 343 (1981)
84. R. Wiltschko, W. Wiltschko, Behav. Ecol. Sociobiol. 9, 135 (1981)
85. W. Wiltschko, R. Wiltschko, W.T. Keeton, R. Madden, Behav. Ecol. Sociobiol. 12, 135 (1983)
86. W. Braemer & Schwasmann, Ergebn. Biol. 26, 182 (1963)
87. C. Groot, Behaviour. Suppl. 14, 198 (1965)
88. S.G. Miles, J. Fish. Res. Bd. Canada 25, 2143 (1968)
89. K. Schmidt-Koenig, Adv. Study Behav. 1, 217 (1965)
90. U. Munro, R. Wiltschko, J. Exp. Biol. 181, 233 (1993)
91. R. Wehner, Ann. Rev. Entomol. 29, 277 (1984)
92. T.H. Watermann, in Photorection and Vision in Invertebrates edited by M.A. Ali (Plenum, 1984), p. 63
93. E.R. Baylor, F.E. Smith, Am. Naturalist 87, 97 (1953)
94. R. Jander, K. Daumer, T.H. Waterman, Z. Vergl, Physiol. 46, 363 (1963)
95. K. von Frisch, Experientia 5, 142 (1949)
96. P. Duelli, R. Wehner, J. Comp. Physiol. 86, 17 (1973)
97. R. Wehner in The Biology of Photoreception edited by D. J. Cosens, D. Vince-Price (Society for Experimental Biology 1983)
98. R. Wehner in Orientation and Communication in Arthropods edited by M. Lehrer (Birkh¨auser, Basel 1997)
99. M. Dacke, M. Byrne, E. Baird, C.H. Schot, E.J. War-rant, Proc. R. Soc. Lond. B. 271, 361 (2004)
100. T.H. Waterman in Light as an Ecological Factor,Vol II edited by G.C. Evans, R. Bainbridge, O. Rackham (Blackwell, Oxford, 1975), p. 305
101. D.H. Taylor, J.S. Auburn, in Animal Migration, Navigation, and Homing edited K. Schmidt-Koenig, W.T. Keeton (Springer, Berlin, Heidelberg, New York 1978), p. 334
102. K. Adler, J.B. Phillips, J. Comp. Physiol. A 156, 547 (1985)
103. M.J. Freake, J. Exp. Biol. 202, 1159 (1999)
104. S. Greif, I. Borissov, Y. Yovel, R. Holland, Nat. Commun. 5, 4488 (2014)
105. M.L. Kreithen, W.T. Keeton, J. Comp. Physiol. 89,83 (1974)
106. K.P. Able, Nature 299, 550 (1982)
107. F.R. Moore, J.B. Phillips, Anim. Behav. 36, 1770 (1988)
108. K.P. Able, M.A. Able, Nature 375, 230 (1995)
109. R. Muheim, J.B. Phillips, S. ˚Akesson, Science 313, 837 (2006)
110. A.J. Helbig, W. Wiltschko, Naturwissenschaften 76, 227 (1989)
111. N. Chernetsov, D. Kishkinev, V. Kosarev, C.V. Bol-shakov, J. Exp. Biol. 214, 2540 (2011)
112. S. ˚Akesson, C. Odin, R. Heged¨us, M. Ilieva, C. Sj¨oholm, A.Farkas,G. Horvath,Biol. Open 4, 35 (2015)
113. W. Wiltschko, R. Wiltschko, U. Munro, H. Ford, J. Comp. Physiol. A 182, 521 (1998)
114. U. Munro, R. Wiltschko, J. Comp. Physiol. A 177, 357 (1995)
115. K.P. Able, M.A. Able, Nature 364, 523 (1993)
116. S.T. Emlen, Auk 84, 309 (1967)
117. Y. Katz, H. Michelsons, H. in Orientazija Ptiz (Orientation of Birds) edited by H. Michelsons, P. Bl¨um & J. Baumaris (Riga, Zinatne 1978), p. 180
118. W. Wiltschko & Wiltschko, Z. Tierosychol. 37, 337 (1975)
119. W. Wiltschko & Wiltschko, Z. Tierosychol. 39, 265 (1975)
120. V.P. Bingman, Behav. Ecol. Sociobiol. 15, 77 (1984)
121. S.T. Emlen, Auk 84, 463 (1967)
122. S.T. Emlen, Science 170, 1198 (1970)
123. W. Wiltschko, P. Daum, A. Fergenbauer-Kimmel, R. Wiltschko, Ethology 74, 285 (1987)
124. K.P. Able, M.A. Able, Nature 347, 378 (1990)
The paper is originally published in The European Physical Journal Special Topics (2022) (https://doi.org/10.1140/epjs/s11734- 022-00610-w) and is republished here with authors’ permission. Copyright: The Authors
To be concluded in December issue.
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