Orientation and Navigation of Migrating Birds

Abstract

The question of how migrating birds find their way to winter quarters and back has fascinated humans since the beginning of scientific research into avian biology. Migrating birds have been shown to possess compass systems that allow them to select and maintain certain compass directions. Three such systems are known, solar, stellar and magnetic. Their details are not quite clear and need further research. Hierarchy and interaction of compass systems of migrating birds are poorly studied; different species may vary in this respect. During migration, birds learn to use maps that make true navigation possible, i.e. to detect their position relatively to the goal of movement. The physical nature of navigational maps is an object of intensive research; currently the most promising concepts are the geomagnetic and possibly olfactory maps. A significant contribution to the study of formation of navigational maps was made by Soviet/Russian researchers, whose work was published in Zoologicheskii Zhurnal (Sokolov et al., 1984). Migrating birds have no innate map, and first-autumn individuals reach their species-specific wintering areas by using compass sense and counting time that should be spent moving in certain genetically fixed directions. However, in recent years more and more data surface that suggest that juveniles (maybe not of all species) do have some mechanism of controlling their position on the migratory route that allows them to compensate for errors of the spatio-temporal programme of migration.

Full text

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ISSN 1062-3590, Biology Bulletin, 2016, Vol. 43, No. 8, pp. 788–803. © Pleiades Publishing, Inc., 2016.
Original Russian Text © N.S. Chernetsov, 2016, published in Zoologicheskii Zhurnal, 2016, Vol. 95, No. 2, pp. 128–146.
100 Years of Zoologicheskii Zhurnal
Orientation and Navigation of Migrating Birds1
N. S. Chernetsov
Biological Station Rybachy, Zoological Institute RAS, Rybachy, Kaliningrad region, 238535 Russia
Department of Vertebrate Zoology, St. Petersburg State University, St. Petersburg, 199034 Russia
e-mail: nikita.chernetsov@gmail.com
Received January 12, 2015
Abstract—The question of how migrating birds find their way to winter quarters and back has fascinated
humans since the beginning of scientific research into avian biology. Migrating birds have been shown to pos-
sess compass systems that allow them to select and maintain certain compass directions. Three such systems
are known, solar, stellar and magnetic. Their details are not quite clear and need further research. Hierarchy
and interaction of compass systems of migrating birds are poorly studied; different species may vary in this
respect. During migration, birds learn to use maps that make true navigation possible, i.e. to detect their posi-
tion relatively to the goal of movement. The physical nature of navigational maps is an object of intensive
research; currently the most promising concepts are the geomagnetic and possibly olfactory maps. A signifi-
cant contribution to the study of formation of navigational maps was made by Soviet/Russian researchers,
whose work was published in Zoologicheskii Zhurnal (Sokolov et al., 1984). Migrating birds have no innate
map, and first-autumn individuals reach their species-specific wintering areas by using compass sense and
counting time that should be spent moving in certain genetically fixed directions. However, in recent years
more and more data surface that suggest that juveniles (maybe not of all species) do have some mechanism of
controlling their position on the migratory route that allows them to compensate for errors of the spatio-tem-
poral programme of migration.
Keywords: birds, migration, orientation, navigation, compass systems, navigational map
DOI: 10.1134/S1062359016080069
INTRODUCTION
Migrating birds annually perform movements for
hundreds and thousands of kilometres, which allows
them to efficiently exploit resources in different cli-
matic zones. Since the first years of scientific research
into avian migration it became apparent that many
birds show breeding site fidelity, i.e. they are able to
return to an area with a radius of several kilometres
after spending winter in hundreds and thousands of
kilometres away (Sokolov, 1991). Considering the dis-
tance of migratory movements, recaptures of tens of
percent of birds at the sites of their previous breeding
obviously cannot result from random processes. If the
birds returned to the immediate area of their hatching
or previous breeding by chance only, recaptures of
individuals marked earlier would have been very rare
events, with just isolated cases over more than a hun-
dred years of bird ringing. The observed return rates in
long-distance migratory songbirds, up to 13% after the
first winter (Bushuev et al., 2012) and 30–40% in
adults (Sokolov, 1991), can only be explained by true
navigation, i.e. finding the goal of migration without
direct sensory contact with it. It has also been shown
that many migratory birds show winter site fidelity at a
level comparable to breeding site fidelity rates
(Mewaldt, 1976; Salewski et al., 2000). Similarly, only
true navigation can explain the ability of many sea-
birds, in particular procellariiforms, to locate small
islands where they breed, after long-distance flights in
the ocean, often involving circumnavigation of the
Earth and lasting for many years (Jouventin and
Weimerskirch, 1990; Åkesson and Weimerskirch,
2014).
In the middle of the 20th century the map and
compass concept was suggested, which assumed that a
migrating (or homing) bird should first detect where it
is located in respect to the goal (or, equivalently, where
the goal is located in respect to it; map step) and then
select and maintain the direction of movement
towards the goal (compass step, Kramer, 1953, 1957,
1961). The ability to use compass, i.e. to select and
maintain a certain compass direction, is called orien-
tation; the ability to use map, i.e. to detect the position
of the goal of movement without direct sensory con-
1The article was translated by the author.

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ORIENTATION AND NAVIGATION OF MIGRATING BIRDS 789
tact with the goal, is called navigation. Generally
speaking, compass systems are necessary not only to
perform migratory movements (Wiltschko, R. and
Wiltschko, W., 2015). Any animal that needs to move
along a straight line for a long period of time (even if
the scale of movements is not very large), needs a
compass system independent of local landmarks. Nav-
igational map that makes it possible to detect the posi-
tion of the goal with which the animal has no sensory
contact (visual, acoustic, olfactory, etc.) is only neces-
sary for the animals that regularly leave their usual
home range and move far beyond it.
It should be emphasized that the map and compass
concept, which has been suggested in the mid 20th cen-
tury and remains a most important theoretical frame-
work of long-distance animal orientation and naviga-
tion research (Wiltschko, R. and Wiltschko, W., 2015),
is not linked to certain mechanisms of orientation and
navigation. The compass system and the navigation
system (map) may be based on different physical prin-
ciples and different sensory modalities. In other
words, the common question “How do migrating
birds find their way?” actually consists of two different
questions (the nature of compass and the nature of
map), and answers to these questions may be different.
METHODS OF ORIENTATION
AND NAVIGATION RESEARCH
The main method of avian orientation and naviga-
tion research are behavioural experiments. As soon as
it became possible to mark birds individually (ringing)
studies of homing success of experimentally displaced
birds started (usually towards the nest). Researchers
had good reasons to assume that at least during the
breeding period the motivation to home to the nest is
high, and interpreted homing success rate as a proxy
for navigation capabilities of a given species or popula-
tion (Rüppel, 1934, 1935; Wallraff, 2005). However,
radio tracking studies showed that the situation is
more equivocal: apart from motivation (which is
impossible to measure directly), there are other phys-
iological factors (e.g. the ability to rapidly change the
diel rhythm of activity) which may influence homing
performance and speed (Mukhin et al., 2009; Mukhin
and Kobylkov, 2014).
Many homing studies have been done in domestic
pigeons (Columba livia f. domestica), because these
birds show a high motivation to return to their loft
regardless of the season. It should be kept in mind
however that wild ancestors of homing pigeons, rock
pigeons, are sedentary birds that perform foraging
flights within several kilometres, up to maximum of
15–20 km. It was questionable whether compass and
especially map cues they use are identical to those used
by migrants for thousands of kilometres.
Significant progress in avian orientation research
was achieved when Gustav Kramer showed that spon-
taneous nocturnal migratory restlessness (Zugunruhe),
whose existence had been known long before the onset
of the scientific bird migration research (Berthold,
1996), is directed (Kramer, 1949). A migratory bird
put in a round cage during the migration season jumps
significantly more often towards the direction to
which it would have moved, were it free-flying. This
discovery made it possible to study spatial orientation
of birds under the controlled lab conditions and
resulted in a significant progress in avian orientation
and navigation research. It would be no exaggeration
to say that birds are the best studied animal long-dis-
tance migrants just because of the behavioural para-
digm that allows lab experiments.
Currently the progress in this field is reached by a
combination of behavioural experiments, both in the
lab in round arena and in free-flying radio-tagged
birds (Cochran et al., 2004; Thorup et al., 2007; Cher-
netsov et al., 2011; Schmaljohann et al., 2013); neuro-
anatomical studies (Heyers et al., 2010; Lefeldt et al.,
2014) and the combination of these methods (Zapka
et al., 2009; Kishkinev et al., 2013). Besides biophysi-
cal research, theoretical work combined with
behavioural experiments make a great contribution to
orientation research, especially to the study of the
magnetic compass (review: Kishkinev and Cher-
netsov, 2015). Research into orientation and naviga-
tion of birds and other animals is without exaggeration
one of the most integrative fields in zoology.
COMPASS SYSTEMS
The current consensus is that avian orientation sys-
tem incorporates redundancy. Usually the existence of
at least three different compass systems is acknowl-
edged: solar compass, based on the apparent move-
ment of the Sun on the sky (Kramer, 1951, 1953;
Schmidt-Koenig, 1990), stellar compass, based on the
pattern of constellations (Emlen, 1967, 1967a; Wiltsc-
hko, W. et al., 1987; Wiltschko, R. and Wiltschko, W.,
2009a), and magnetic compass, based on the lines of
the geomagnetic field (Wiltschko, W. and Wiltschko, R.,
1972). The proposed use of other cues for selecting
and maintaining compass directions, e.g. the moon,
has not been proven and is questionable (Wiltschko, R.
and Wiltschko, W., 1999).
Solar and stellar compasses are sometimes lumped
under the name of astronomical cues, as both of them
are based on the apparent rotation of the celestial bod-
ies and on the visual system. They are contasted with
the magnetic compass which is based on radically dif-
ferent principles and utilises an own sensory system
(magnetoreception; Mouritsen, 2013, 2015). How-
ever, a detailed analysis shows that solar and stellar
compasses differ significantly, and lumping them
together is probably not justified.

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Solar Compass
Solar compass is based on the regular apparent
movement of the Sun across the sky from the east to
the west via south (in the Northern Hemisphere) or via
north (in the Southern Hemisphere). Using this regu-
lar movement for detecting compass direction is only
possible when taking the time of the day into account,
i.e. solar compass is time-dependent. In the Northern
Hemisphere at solar noon the sun is exactly in the
south—but to use this information, one should know
when the solar noon is.
Furthermore, for the efficient use of the solar com-
pass it is necessary to account for the non-uniform
rate of solar azimuth change: just after sunrise, the Sun
rapidly climbs, and just before sunrise, it rapidly
descends, with a low rate of horizontal movement
(azimuth change). Conversely, around solar noon, the
elevation of the Sun above the horizon changes slowly,
and the azimuth changes more rapidly than in the
morning and in the evening. The form of the solar arch
depends on the geographic latitude and on season.
As it is not possible to experimentally manipulate
the position of the Sun, and a realistic imitation in a
planetarium is challenging, most studies of the solar
compass have been performed by clock shifting. The
birds are for a sufficient period of time kept in an arti-
ficial photoperiod which is shifted by several hours as
compared with the natural one. When the internal
clock of the birds is synchronised with this artificial
photoperiod, the birds are tested outdoors in sunny
weather. It is not possible to move the Sun, but one
can shift the animal’s internal clock, which gives an
equivalent result in the case of a time-dependent com-
pass mechanism. When interpreting the results of such
tests, one must take the non-uniform movement of the
Sun into account. Many authors assume that shifting
the clock by 1 hour results in the solar compass being
offset by 15°. This assumption is, generally speaking,
not correct: in summer at 50° N, a six-hour clock shift
may offset the solar compass by as much as 130°
(Wiltschko, R. and Wiltschko, W., 2015). The experi-
ments in homing pigeons showed that these birds
account for that (Wiltschko, R. et al., 2000). Moreover,
pigeons when using the solar compass, consider only
the azimuth of the Sun and ignore its elevation above
the horizon (Schmidt-Koenig, 1958; Keeton, 1979).
Most research into solar compass of birds has been
done in homing pigeons (Schmidt-Koenig, 1958;
Keeton, 1979; Wiltschko, W. et al., 1976, 1984). The
reason is that clock shifting experiments are easier to
perform in the behavioural context of homing, and
homing is easier to study in pigeons. To clock shift a
songbird, one has to take it into captivity for several
days (Mukhin et al., 2009), which may significantly
impact its motivation to return to its nest. Therefore
most studies of solar compass in passerines have been
done in a non-migratory behavioural context (Wiltsc-
hko, W. and Balda, 1989; Duff et al., 1998; Wiltschko, W.
et al., 1999). It has been even suggested that solar com-
pass exists but is not used by the birds for migratory
orientation (Wiltschko, R. and Wiltschko, W., 2015).
This viewpoint is difficult to support: at least some
migrating birds, e.g. grey-cheeked thrushes (Catharus
minimus) and Swainson’s thrushes (C. ustulatus),
select the direction of migratory flights on the basis of
the information derived from sunset cues (i.e. basically
from the sun), but maintain the direction by magnetic
compass (Cochran et al., 2004). The existence of such
a mechanism has been also proposed for other song-
bird species, e.g. for American sparrows (Muheim
et al., 2006a, 2007, 2009), but for thrushes it has been
proven beyond reasonable doubt.
Apart from the time-dependent solar compass,
another method of determining cardinal directions
from the movement of the Sun has been proposed
(Muheim et al., 2006a). This hypothetical method is
based on the idea that if a bird detects (directly or from
the band of maximum polarisation on the sky) the
sunset point and remembers its position, and then,
without changing its position, detects the sunrise
point, it would be able to find the bisector of the angle
between the sunset and sunrise directions. This bisec-
tor is always, in any season and everywhere on earth
(except of the geographic poles, but they are not very
relevant for migrating birds), the north—south axis.
This method of orientation with the help of the Sun is
very simple and elegant, but the claim that it is sup-
ported by the experimental data (Muheim et al.,
2006a) is erroneous (Liu and Chernetsov, 2012). The
existence of this time-independent form of the solar
compass is still pending confirmation.
Most probably, the classic time-dependent solar
compass is used by the birds, primarily by diurnal
migrants, for orientation. The paucity of supporting
data is probably due to the methodological difficulties
of studying solar compass in the migratory context and
to the difficulty of using round arenas for the study of
directedness of diurnal migratory activity.
Stellar Compass
The second celestial compass system used by
migratory birds is the star compass. The ability of
migratory birds to orient by the pattern of the starry
sky was demonstrated soon after the discovery of the
sun compass (Sauer, F., 1956, 1957) and subsequently
confirmed by various authors (Katz and Mihelson,
1978; Bingman, 1984, 1987; Mouritsen and Larsen,
2001). It was initially assumed that birds derive posi-
tional information from the stars (Sauer, F., 1957;
Sauer, E.G.F. and Sauer, E.M., 1960), but soon it was
shown that this was not the case: stellar information is
used for compass orientation, but is not a component
of map (Wallraff, 1960).
It was shown in the 1960s that the star compass of
migrating birds undergoes a complex ontogenetic

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ORIENTATION AND NAVIGATION OF MIGRATING BIRDS 791
development (Emlen, 1967a). During the pre-migra-
tory period, juvenile indigo buntings (Passerina cya-
nea) learn to find the centre of rotation of the starry
sky located near the Polaris, which in the northern
hemisphere shows the direction towards geographic
North. By the moment of starting autumn migration,
indigo buntings in the experiments of Stephen Emlen
had learned to use the pattern of constellations to deter-
mine the geographic North, and no longer needed the
rotation. Birds raised in the planetarium under the sky
that was rotated around Betelgeuse (αOrion), under
the natural autumnal sky considered the direction
towards Betelgeuse to be the North and offset the inher-
ited population-specific autumn migratory direction
from this false “North” (Emlen, 1967a, 1970). They did
not care that the sky was rotating in a different fashion
as compared to their pre-migratory periods, i.e. stellar
rotation was no longer used as a reference.
Stephen Emlen performed his experiments in a
planetarium which provided a rather realistic imita-
tion of the starry sky (Emlen, 1970). Further studies
showed that a rather rough imitation (just 16 light
dots) is already sufficient for juvenile migrants and
allows them to find the rotation centre and to learn to
offset the directions from it, “believing” that it is the
North (Wiltschko, W. et al., 1987; Able, K.P. and
Able, M.A., 1990; Weindler et al., 1997). The birds
learn to find the North without observing the slow
motion of the stars, but just on the basis of the learned
geometric pattern of the light dots (real stars or their
imitation). Stellar compass developed this way no lon-
ger needs celestial rotation to operate (under the sta-
tionary sky in the planetarium the birds orient exactly
the same as under the rotating one) and is time-inde-
pendent (Emlen, 1970; Wiltschko, W. et al., 1987;
Weindler et al., 1997), which makes it significantly
distinct from the solar compass.
The ontogenetic development of the stellar com-
pass in indigo buntings described by Stephen Emlen is
astonishingly complex. Its use demands well devel-
oped cognitive abilities, much more sophisticated
than the use of the magnetic compass, which usually
amazes humans most. The magnetic compass is based
on the insufficiently studied sensory modality absent
in humans, which is on top of that probably based on
rather subtle quantum mechanical processes (Krylov
et al., 2014; Kishkinev and Chernetsov, 2015). How-
ever, stellar compass cannot function without devel-
oped cognitive abilities (Chernetsov, 2015). In partic-
ular, the birds need to detect a very slow rotational
motion of the sky (15° per hour) and to identify the
centre of rotation, which is a non-trivial cognitive task
(Mukhin, 1999; Alert et al., 2015). The ontogenetic
development of this compass system has been shown
in garden warblers (Sylvia borin) as well as indigo bun-
tings (Wiltschko, W. et al., 1987; Weindler et al., 1997).
In a number of cases researchers failed to show a work-
ing star compass formed during observations of the
rotating sky, possibly due to phototactic artefacts
which are difficult to avoid in captivity (Michalik
et al., 2014).
Besides, the time-independent nature of the devel-
oped stellar compass actually remains to be formally
shown. This feature of the star compass, which makes it
distinct from the sun compass, has been shown in indigo
buntings (Emlen, 1967a) and confirmed in the experi-
ments in pied flycatchers (Ficedula hypoleuca) and black-
caps (Sylvia atricapilla) (Mouritsen and Larsen, 2001).
However, both these studied were performed in the mag-
netic field which was disturbed as compared with the nat-
ural one, but could provide directional information.
Probably the developed star compass of migrating birds
indeed does not need a correctly synchronised internal
clock to function properly, but this remains to be demon-
strated.
Magnetic Compass
Magnetic compass is the third independent com-
pass systems of migrating birds. This compass is based
on a sensory modality which is not present in humans;
therefore, its use amazes researchers. This was proba-
bly the reason for the scepticism which met the
authors of the first reports on the use of geomagnetic
information by migrating birds (Merkel and Wiltsc-
hko, W., 1965; Wiltschko, W., 1968). Authorities on
bird migration wrote that “studies in the non-celestial
orientation of birds are not more successful than the
studies of human telepathy. Fading and again reviving
interest to this field is fuelled by the interest to the
enigmatic and mystical” (Dolnik, 1973). The situation
changed when a key paper was published in Science,
which reported the existence and the inclination
nature of the magnetic compass in European robins
(Erithacus rubecula) (Wiltschko, W. and Wiltschko, R.,
1972), and when the proponents and the opponents of
the magnetic orientation performed a joint study and
published results that convincingly showed that the
former group had been right (Emlen et al., 1976).
Currently the existence of the magnetic compass
systems in birds is not questioned by serious research-
ers. There are also reports on using magnetic compass
by mammals (Burda et al., 1990; Deutschlander et al.,
2003; Holland et al., 2006), sea turtles (Lohmann, K.J.,
1991; Lohmann, K.J. and Lohmann, C.M.F., 1993),
amphibians (Deutschlander et al., 1999; Diego-
Rasilla et al., 2010, 2013) and bony fishes (Quinn
et al., 1981). The sensory mechanism of the magnetic
compass of animals remained unknown for a long time
after its discovery, but significant progress has been
achieved in this field in the last 15–20 years (Wiltsc-
hko, R. and Wiltschko, W., 2015).
The most widely held theory is that the detection of
geomagnetic compass information is based on the per-
ception of the magnetic field through light-dependent
biradical chemical reactions, the receptor molecule is
a cryptochrome protein, and magnetoreception takes

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CHERNETSOV
place in the retina. As a result, geomagnetic field is
perceived as a visual image, i.e. birds literally “see” the
magnetic field (Solov’yov et al., 2010; Mouritsen, 2013,
2015). For detailed reviews of the working mechanism of
the avian magnetic compass, the readers are referred to
earlier publications (Kishkinev and Chernetsov, 2015;
Krylov et al., 2014). However, it should also be men-
tioned that it has recently been shown that the biophysi-
cal model of biradical magnetoreception suggested earlier
(Schulten et al., 1978; Ritz et al., 2000) cannot explain
some experimental effects (Kavokin, 2009; Kavokin et
al., 2014; Engels et al., 2014) and needs to be modified.
Most probably, the general working principles of the
magnetic compass are correctly described by the current
model, but some important points need clarification and
possibly correction.
The magnetic compass, unlike solar and stellar
compasses, is believed to be innate and not learned. As
it does not involve the movement of celestial bodies,
the magnetic compass can be used 24 hours a day and
does not depend on the animal’s internal clock. Light-
dependence of the magnetic compass means that it
cannot function in complete darkness, but illumina-
tion characteristic of a starry moonless night, is suffi-
cient. One may think that it is a perfect compass
mechanism which makes celestial cues obsolete.
However, it should be kept in mind that magnetic
poles do not coincide with geographic ones, so the
direction towards the magnetic North is generally
speaking not the same as the direction toward the geo-
graphic North. The angle between these two direc-
tions, known as magnetic declination, may vary
between –20°…+20° in the areas regularly frequented
by migrating birds (Fig. 1). As a result some migrants,
e.g. a Swainson’s thrush population breeding in Alaska
(declination +20°) and wintering in northern South
America (declination –10°; Delmore et al., 2012;
Ruegg et al., 2014), visit areas where the true geo-
graphic azimuth of the magnetic North varies by 30°.
Such an error of the compass systems is unacceptable.
A bird from such a population would not be able to
successfully solve orientation tasks during its annual
cycle if it only uses a magnetic compass.
Hierarchy and Integration of Compass Systems
The redundancy of information provided by com-
pass systems apparently demands a hierarchy and inte-
gration rules. It has been repeatedly shown that even
though the magnetic compass is believed to be innate,
its successful use during migration in many bird spe-
cies depends on the ability to observe celestial rota-
tion, diurnal (Able, K.P. and Able, M.A., 1990a, 1993;
Weindler et al., 1998) or nocturnal (Emlen, 1970; Shu-
makov and Zelenova, 1988; Able, K.P. and Able, M.A.,
1990; Weindler et al., 1995; Michalik et al., 2014).
Birds that had not been able to observe celestial rota-
tion during their growth phase before the onset of first
Fig. 1. Map of the isolines the magnetic declination (isogones). Based on the data of U.S. NOAA National Geophysical Data
Center and Cooperative Institute for Research in Environmental Sciences; source: http://ngdc.noaa.gov/geomag/WMM/data/
WMM2015/WMM2015_D_MERC.pdf. Isogones are shown after every 2° of declination.
0
70°
15°
30°
30°
45°
60°
70°
45°
60°
15°
180°
0°
135°13 5 °180°90°90°45°45°0°
20
10
20
10
−10
−10
−30
−20
−10
0
−20
−10
−10
10
20
−20
20
30
40
50
0
0
−30
−60
−70
−80
−110
−120
−130
−100
−90
0
20
30
40
50
60
70
80
10
70
60
100
130
110
80
90
50
40
30
20
10
10
10
0
N
W

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ORIENTATION AND NAVIGATION OF MIGRATING BIRDS 793
migration, when tested in the natural magnetic field
without access to astronomical cues either were disori-
ented, or showed a bimodal orientation along the
migratory axis, i.e. were not able to select the correct
end of the axis. Juvenile European robins that had
been allowed to observe the imitated rotation of the
sky for three weeks, proved able to calibrate their mag-
netic compass, whereas the birds that had observed the
rotation for one week or less, were disoriented like
those that did not see the rotating sky at all (Michalik
et al., 2014). Not only the duration of exposure under
the rotating celestial sphere in the post-juvenile
period, but also exposure in the certain sensitive
period may have played a role; similarly to the forma-
tion of the navigational map of “home,” to which a
bird returns after its first non-breeding season (Löhrl,
1959; Sokolov et al., 1984, 1987). The general pattern
seems to be that before the onset of first migration, the
magnetic compass of songbirds is calibrated by the
celestial rotation. It is noteworthy that in this particu-
lar case the solar compass (based on the movement of
the Sun), and the rotation of the stars behave as a sin-
gle celestial compass system.
During migration the interaction of compass sys-
tems looks different. Many authors have reported the
results of their cue conflict experiments, during which
they manipulated either magnetic or celestial informa-
tion (by mirrors or polarising filters). The results were
conflicting (see reviews Muheim et al., 2006; Liu and
Chernetsov, 2012). In some cases migrants calibrated
the celestial (stellar) compass from the magnetic one
(Wiltschko et al., 1998, 1999; Sandberg et al., 2000), in
others, conversely, the direction was selected from
sunset cues and maintained during nocturnal flight,
when neither the Sun nor the polarisation pattern are
visible, by the magnetic cues (Moore et al., 1985;
Cochran et al., 2004; Muheim et al., 2006a, 2007,
2009). In some experiments compass systems did not
interact at all, and simple domination of one of the
compasses was observed, i.e. the wrong readings of the
experimentally manipulated compass systems were
simply ignored (Katz and Mihelson, 1978; Wiltschko, R.
et al., 2008; Chernetsov et al., 2011; Schmaljohann
et al., 2013; Åkesson et al., 2015). In some cases the
same team of researchers in the same model species
obtained contradicting results by different methods
(Gaggini et al., 2010; Guinchi et al., 2015).
It should be emphasized that this complex and
intricate pattern should not be interpreted to mean
that nothing is certain or that many, if not most, stud-
ies are erroneous and should be discarded. Even
though many authors have criticised the approaches of
their colleagues, possibly sometimes with reason
(Wiltschko, R. et al., 2008, 2008a; Muheim et al.,
2008), at least some studies are performed very rigor-
ously so that their results are highly unlikely to be
caused by artefacts. For example, it is difficult to find
any flaws in the study by Cochran et al. (2004) which
found that grey-cheeked and Swainson’s thrushes
select the direction of their nocturnal migratory flights
by sunset polarisation information, and maintain it by
the magnetic compass (i.e., that they calibrate the
magnetic compass from solar cues). No less convinc-
ing are the studies that demonstrated that song
thrushes (Turdus philomelos) and Northern wheatears
(Oenanthe oenanthe) do not do that (Chernetsov et al.,
2011; Schmaljohann et al., 2013) but show a simple
domination of one of the compass systems, most prob-
ably the magnetic one.
The most parsimonious explanation of these
diverse results is, in our opinion, the suggestion that
compass system hierarchy differs between the species
of migrants, or even between populations within spe-
cies. Some birds, for instance those that perform long-
distance migrations and cross the areas with very dif-
ferent magnetic declination values, have to regularly
check their magnetic compass from the celestial one.
Other species that migrate shorter distances or even
longer flights which remain within similar declination
values (noteworthy, declination does not need to be
close to zero; it suffices if it is relatively uniform
throughout the route), do not need this cognitively
challenging system and get by with the magnetic (or
stellar) compass alone. Furthermore, mortality risk of
an orientation error is much different for a bird that
migrates for short or medium distance over land, with-
out crossing major ecological barriers (e.g., a Euro-
pean robin or a chaffinch (Fringilla coelebs) from a
Baltic population; Payevsky, 1971), than for a bird that
crosses deserts or oceans and winters in relatively small
islands (e.g. for a bar-tailed godwit (Limosa lapponica
baueri) flying from Alaska to New Zealand (Gill et al.,
2009)). In the former case a directional error of 5° or
even 10° may have no negative consequences, whereas
in the latter case an error of 30′ is fatal. If natural selec-
tion forces different species and populations of
migrants to solve navigational and orientation tasks of
varying complexity, it is to be expected that the real-
ised systems will differ, even if sensory basis of orien-
tation is similar or identical. Selection will not shape
“the perfect navigator” (just like it does not support
“the perfect flying machine”; Dolnik, 1995), but will
support the accuracy of orientation and navigation
that is sufficient for population survival.
It may also be the case that some migratory birds
may secondarily lose some orientation systems, or, to
put it more cautiously, these systems may function sig-
nificantly worse in some species than in others (Cher-
netsov, 2015). Some data suggest that not all species of
migrants may successfully use all three compass sys-
tems (solar, stellar and magnetic): garden warbler
devoid of access to geomagnetic information at sunset
(i.e., unable to calibrate the magnetic compass from
sunset cues), were disoriented during the deep night,
even if they had access to the correct stellar informa-
tion (Pakhomov and Chernetsov, 2014). This certainly
makes the pattern even more complex.

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NAVIGATIONAL MAP
Unlike compass systems, about which relatively
much is known (even though, as we have just shown,
many questions remain), the physical nature of the
navigation system (the map) is much less clear. There
are two main concepts of how the map could be organ-
ised. One of them is the mosaic map concept (Wallraff,
1974), which assumes that an animal remembers a
network of local cues around the area it needs to return
to in the future. These local cues, or beacons, may be
landscape ones (visual), or perhaps olfactory or mag-
netic ones. Most humans use the mosaic map when
moving across a familiar terrain: we know how to walk
or to dri ve from a s ubway sto p to ou r home, from hom e
to the nearest supermarket or to school, etc.
Mosaic map is not identical to a cognitive map sensu
Tolman (1948) and subsequent authors (O’Keefe and
Nadel, 1978). A cognitive map concept assumes that
an animal has a mental representation of the geomet-
ric parameters of an area and thus can take novel
routes (make shortcuts) between localities in this area.
A mosaic map suitable for navigation may not have
these qualities.
Another variant is the gradient map concept (Wall-
raff, 1974). This concept assumes that birds (or other
animals) measure a gradient that regularly and pre-
dictably varies along a spatial scale comparable to the
scale of the intended movement, or ideally, slightly
beyond the scale of the movement. The gradient may
be of geomagnetic field parameters (total intensity,
inclination and declination), or possibly of concentra-
tions of certain volatile compounds in the atmosphere.
Unlike a mosaic map, which probably cannot be used
at distances exceeding several tens of kilometres, a gra-
dient map can potentially be used for navigation across
hundreds and thousands of kilometres. To do that,
migrating birds need a bicoordinate grid of two inter-
secting gradients, roughly equivalent to geographic
latitude and longitude.
The use of migrating birds of a gradient map, at
least at the scale of several kilometres or tens of kilo-
metres, has been demonstrated in an important field
experiment performed by Sokolov and colleagues on
the Courish Spit on the Baltic coast (Sokolov et al.,
1984). The authors showed that in order to be able to
return to their natal area in the subsequent year, juve-
nile chaffinches must be able to move freely across
that area. The birds that were kept in a semi-open
pavilion until 50–70 days old, and then moved beyond
their natal area and released, proved unable to return.
It seems that to form bonds with the natal area (i.e., to
form a map), chaffinches need to move at least at the
scale of several hundred metres or several kilometres
and to sample some physical gradients.
As for the physical basis of navigation map, the
most popular and actively discussed possibilities are
currently the olfactory and the magnetic map (Kishki-
nev, 2015). Apart from these two hypotheses, infra-
sound and gravitational anomalies are also suggested
as the source of navigational information. However,
these concepts are seriously discussed by a smaller
number of researchers.
Olfactory Map
Olfactory map as a source of map information was
first suggested by Papi and co-authors (Papi et al.,
1971, 1972) and has been actively discussed over the
last 40 years (Wallraff, 1999, 2005; Gagliardo, 2013).
Most experimental evidence supporting this theory
has been obtained in homing pigeons. In a nutshell,
birds deprived of olfactory information (e.g., by plug-
ging their nostrils, destroying the olfactory epithelium
by washing the nostrils with zinc sulphate ZnSO4 solu-
tion, application of local anaesthesia, or, most radi-
cally, by ablation of the olfactory nerve) perform much
poorer during homing to their loft than control birds
(for a review, see Wallraff, 2005). This affects all of the
main parameters that are commonly used for estimat-
ing homing efficiency in pigeons: scatter of vanishing
directions, returning time and the proportion of
returning individuals. Many early experiments were
performed without correct controls (Wallraff, 1980,
1981), which provided reasons to criticise the olfactory
map concept. In recent years proponents of the olfac-
tory map published the results of new experiments
with all the necessary controls (Gagliardo et al., 2006,
2008, 2009). These experiments showed that only
pigeons with intact olfactory nerves were able to home
successfully, whereas the pigeons with the ablated
nerve proved unable to solve this task. Ablation of the
ophthalmic branch of the trigeminal nerve (V1),
which is believed to transmit the magnetic information
to the brain (Mora et al., 2004; Heyers et al., 2010;
Lefeldt et al., 2014), did not influence homing perfor-
mance in pigeons. Similar results were obtained in
Cory’s shearwaters (Calonectris borealis): these birds
also use information transmitted via the olfactory
nerve for homing, but can return to the colony without
V1-transmitted information (Gagliardo et al., 2013).
The ability of procellariiforms to home successfully
without geomagnetic information had been earlier
independently shown by various authors (Benhamou
et al., 2003; Bonadonna et al., 2003; Mouritsen et al.,
2003).
It should be mentioned however that the olfactory
hypothesis is still being criticised. The main issue is
that it is difficult to understand which volatile com-
pounds could enable the existence of sufficiently sta-
ble gradients across tens, hundreds and even thou-
sands of kilometres. Modelling has shown that over
the ocean, where atmospheric flows are more stable
and predictable, such gradients are more or less imag-
inable, whereas in continental areas the olfactory
landscape is too dynamic to be used to navigation
(Waldvogel, 1987). The proponents of the olfactory
concept object and maintain that the current data

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ORIENTATION AND NAVIGATION OF MIGRATING BIRDS 795
show that the concept is realistic from the viewpoint of
atmospheric physics (Wallraff and Andreae, 2000;
Wallraff, 2013), but this issue cannot be considered
resolved. The existing experimental evidence of olfac-
tory map use mainly refers to seabirds and homing
pigeons. It is conceivable that over the ocean, smell
gradients indeed play an important role in navigation;
in the case of homing pigeons, one may assume that
the olfactory navigational abilities of their sedentary
wild ancestors were hypertrophied by artificial selec-
tion. The experiment with grey catbirds (Dumetella
carolinensis) stands apart. Grey catbirds displaced by
1000 km from their migratory route were unable to
compensate for the displacement if their olfactory epi-
thelium had been degraded by zinc sulphate solution
(Holland et al., 2009). The lead author himself agreed
that it is difficult to imagine stable olfactory gradients
enabling navigation at this spatial scale, and called
these results surprising (Holland, 2014).
One should also mention the so-called activation
hypothesis, which suggest that smells per se are not
used by homing pigeons for navigation, but instead
activate some “independent non-olfactory naviga-
tional system” (Jorge et al., 2009, 2010). According to
these authors, any strong unusual olfactory stimuli,
including obviously artificial ones and not carrying
any navigational information (e.g. lavender or euca-
lyptus smells), may “activate” the navigational system
of pigeons. This hypothesis triggered a discussion
(Gould, 2009; Gagliardo et al., 2011; for a review see
Wallraff, 2014); in our opinion, its weaknesses have
been analysed in sufficient detail in the aforemen-
tioned review, to which an interested reader is referred.
Magnetic Map
The magnetic map hypothesis is, in our opinion, a
well-founded one. It should however be emphasised
that even though this hypothesis has been repeatedly
discussed by different authors (Gould, 1989; Phillips,
1996; Walker et al., 2002; Freake et al., 2006; Kishki-
nev, 2015) and is believed by many non-specialists in
animal navigation to be an established fact, at least in
respect to migrating birds it is still (as of yet) a hypoth-
esis, and not a theory proven beyond reasonable
doubt. A crucial piece of evidence could be data of an
experiment with virtual magnetic displacement, in
which the birds kept in the artificial magnetic field corre-
sponding to the natural field parameters in a remote
location show a predictable orientation response to the
magnetic stimulus, e.g. re-orientation consistent with
the compensation of virtual displacement. The mag-
netic field should be the only parameter altered, and
all other potential navigational cues (smells, photope-
riod, access to celestial cues, etc.) should be the same.
Such data have been recently obtained by us (Kishki-
nev et al., 2015). Disorientation of birds in response to
magnetic displacement, obtained in some experiments
(Fischer et al., 2003; Deutschlander et al., 2012), can be
claimed to be a non-specific response and cannot be
treated as hard evidence in favour of a magnetic map.
The geomagnetic map hypothesis assumes that
migrating birds use a gradient map which is based on
the regular variation of the geomagnetic field parame-
ters: total intensity and magnetic inclination. Both
these parameters generally vary from the poles to the
equator: total field intensity is the highest (ca. 60000 nT)
at the geomagnetic poles and the lowest (ca. 30000 nT,
locally down to 24000 nT) at the magnetic equator;
inclination is +90° at the northern magnetic pole, 0°
at the magnetic equator (i.e., field lines are parallel to
the surface of the Earth; which is the definition of the
magnetic equator) and –90° at the southern magnetic
pole (Skiles, 1989). However this is a very broad
description; in reality the isolines of total intensity and
inclination do not run exactly parallel to the geo-
graphic parallels and to each other (Fig. 2). In some
regions (e.g. in the Indian Ocean) isolines of both
parameters form a grid usable for bicoordinate purely
magnetic navigation (north—south and east—east);
however, in other large areas, e.g. in southern North
America and in Australia, they run parallel to each
other and provide no east—west information
(Boström et al., 2012).
Therefore, a geomagnetic map based on total
intensity of the field and on inclination, may provide a
bicoordinate navigation grid in some regions but not
everywhere on Earth. If the birds can detect not only
total intensity and inclination, but also declination,
the longitude problem (east—west axis) will be com-
pletely solved, and bicoordinate navigation provided
(Skiles, 1989; Fig. 1). In principle, migratory birds
have a sensory basis for measuring declination, and
they should use a magnetic and a celestial (solar or
stellar) compass and compare the readings. In this
case the map is not purely geomagnetic, but magnetic-
celestial, as one of the gradients is measured by an
astronomic compass. However, the ability to detect
declination and to use it as a map element remains to
be demonstrated in migratory birds.
Unlike the magnetic declination, the ability of
birds to detect total intensity and inclination has been
shown. Operant conditioning experiments showed
that pigeons can respond to simultaneous strong
change in intensity and inclination (Mora et al.,
2004), when this information is transmitted to the
brain via V1, and also to the change in inclination
alone (Mora et al., 2014). Similar results have been
obtained in Pekin ducks (Anas platyrhynchos f. domes-
tica; Freire et al., 2012). We were able to show that the
ability of Eurasian reed warblers (Acrocephalus scirpa-
ceus) to compensate for the physical displacement by
1000 km along longitude is critically dependent of
receiving V1-transmitted information (Kishkinev et al.,
2013). Intact reed warblers are able compensate for the
displacement (Chernetsov et al., 2008), and also
sham-operated birds, whereas V1-ablated individuals

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CHERNETSOV
continued to show the same orientation as they had
done before the displacement (Kishkinev et al., 2013).
Even though we did not show the nature of the infor-
mation transmitted through V1, indirect evidence sug-
gests that this information is magnetic. Taken
together, these data in our opinion strongly suggest
that (1) migrating birds can perceive information on
intensity and direction of the geomagnetic field;
(2) this information is transmitted to the brain via V1;
(3) this information is used for position finding at the
scale of hundreds and thousands of kilometres. Clear
evidence of the existence of a magnetic (or magnetic-
celestial, see above) map in migratory birds would be
shown by successful and repeatable experiments with
virtual magnetic displacement with a predictable ori-
entation response, similar to the response to the real
displacement (Kishkinev et al., 2015).
It should be noted that the structure of the putative
V1-innervated magnetoreceptors remains unknown
(a review: Kishkinev and Chernetsov, 2015). However,
there is indirect evidence that such receptors exist
(Mouritsen and Hore, 2012) and transmit information
on intensity and inclination of the magnetic field
(Mora et al., 2004; Heyers et al., 2010; Lefeldt et al.,
2014), which might be used for long-distance naviga-
tion (Kishkinev et al., 2013). However, the structure
and the exact location of these receptors remain
unknown; previously suggested opinions on that topic
appeared to be erroneous (Treiber et al., 2012).
If the geomagnetic map exists, the question of its
spatial accuracy inevitably follows. Difference
between total field intensity at the poles and at the
equator is ca. 30000 nT; the distance between the pole
and the equator is ca. 10000 km. Thus, the mean gra-
dient of field intensity is 3 nT/km. At the same time,
daily variation of the field is tens of nT, and magnetic
storms can alter the field by hundreds and in excep-
tional cases up to 1000 nT (Skiles, 1989). This means
that the spatial accuracy of the magnetic map is ca.
25–50 km (at smaller scale noise becomes stronger
than signal), whereas the accuracy of avian navigation
is considerably higher, roughly by an order of magni-
tude (Sokolov, 1991). Either migrating birds use rather
sophisticated algorithms of isolation of signal from
noise, or avian position finding is a hierarchical pro-
cess using a magnetic map at large scale and some
other mechanism at smaller scale.
Other Navigation Systems
Apart from the putative olfactory and magnetic (or
magnetic-celestial) maps, other positioning cues have
been suggested as sources of information for avian
maps. At an early stage, the proposal that birds use the
Coriolis force was forwarded (Yeagley and Whitemore,
1947). This suggestion has not been treated seriously
for a while and now belongs in history of science.
Anther exotic hypothesis, namely that pigeons use
gravitational anomalies for navigation, is still being
Fig. 2. Map with isolines of total intensity of the geomagnetic field (isodynamic lines, light grey, in μT) and of magnetic inclina-
tion (isoclines, dark grey, in degrees). Mercator map projection, revised from Boström et al. (2012). Isodynamic lines and iso-
clines may form a good grid (e.g. in Siberia or in the Indian Ocean), or may run nearly parallel to each other (North America,
Australia).
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ORIENTATION AND NAVIGATION OF MIGRATING BIRDS 797
debated (Larkin and Keeton, 1978; Kanevskyi et al.,
1985; Blaser et al., 2013, 2014). The idea is that birds
can detect heterogeneities in the gravitational field of
the Earth generated by varying density of the rocks,
and use it as a source of map-related information (or
perceive it as a disturbance). The main issue with this
hypothesis is not that all evidence invoked in its sup-
port is purely correlational (considering the nature of
gravitational force, a controlled experiment is hardly
conceivable), and not even that using a gravitational
map would demand that pigeons should discriminate
the angles of the gravitational force direction differing
by several angular seconds. It is that to detect gravita-
tional anomalies, one should be able to sense the
downward direction (i.e., towards the centre of the
Earth’s gravitational mass) in a given point, and also
simultaneously compare it with the downward direc-
tion in a remote location. This ability is not provided
by the vestibular system, either avian or human; other-
wise we would have detected that “downward” direc-
tions in St. Petersburg and Vladivostok are much dif-
ferent, and upon disembarking a f light from Europe to
New Zealand, we would have felt that we walk upside
down. Lacking ability to detect the frozen direction
“downward at home,” independent from the local
downward direction in any animal, forces one to treat
the gravitational hypothesis as a curiosity, in spite of
recent publications in respectable journals (Blaser
et al., 2013, 2014).
Among the “non-traditional” navigation hypothe-
ses the most credible one looks at the use of infrasound
(Hagstrum, 2001, 2003, 2013). Some landscape struc-
tures, for instance mountain ranges and especially sea
coasts, generate the constant infrasound with frequen-
cies between 0.1–10 Hz, which might be used as a
source of spatial information by animals, including
birds that are able to perceive it. There are correlative
data that homing efficiency of pigeons is changed
during natural or anthropogenic infrasound distur-
bances (Hagstrum, 2000). The infrasound hypothesis
looks much less exotic than using Coriolis force or
gravitational anomalies. Infrasound can hardly be the
main source of positional information for long-dis-
tance migrants, because it does not form a grid, but its
use by some birds as one of local landscape cues is pos-
sible and does not violate the known laws of nature.
Finally, one of the first position-finding hypothe-
ses ever suggested was the astronomical navigation
concept, based on observations of apparent move-
ments of the Sun and the stars (Matthews, 1953; Sauer, F.,
1957; Sauer, E.G.F. and Sauer, E.M., 1960). These
hypotheses did not find support in subsequent studies.
It is currently accepted that both the Sun (Schmidt-
Koenig, 1961, 1990) and the stars (Mouritsen and
Larsen, 2001) provide migrating birds only with com-
pass information. In particular, to use the Sun or the
stars for true navigation the birds would need to detect
their position in the sky with a high precision, and it is
not clear whether they are capable of that (Hodos,
1993). Furthermore, experimental evidence does not
support the celestial navigation hypothesis.
Spatio-Temporal Programmes and Controlling
the Position on the Migratory Route
Since the classic experiments of Perdeck on star-
lings (Sturnus vulgaris) (Perdeck, 1958) it is usually
assumed that experienced adult migrants performing
migration not for the first time use a navigation map,
whereas juvenile birds migrating for the first time have
no map (in the Northern Hemisphere it usually hap-
pens in autumn). It is believed that first-autumn
migrants flying towards their winter quarters where
they have never been before, do not use a map, which
in birds is not innate, but experience-based, but follow
an innate spatio-temporal programme (Gwinner and
Wiltschko, 1978). This programme in the simplest way
may be formulated as “start migration at a certain age,
fly towards the direction α during n days, then fly
towards β during m days, etc.; in the end you have
reached your destination (winter area).” First-autumn
migrants are believed to have no idea in which part of
their route they currently are. This idea is called “clock
and compass” concept, even though a more accurate
name would be “calendar and compass.” The main
point is that it does not include an innate map.
This concept is the most influential and widely
held view currently. A number of facts agree with it:
experiments with white-crowned sparrows (Zonotri-
chia leucophrys) displaced from the northwestern to
the northeastern U.S. confirmed the ability of adult
experienced migrants to detect and compensate for a
longitudinal displacement and the inability of juve-
niles to do it (Thorup et al., 2007). The geographic
distribution pattern of long-distance recoveries of
ringed pied flycatchers is exactly the same as should be
expected if during their first autumn these birds use a
clock and a compass and do not compensate for the
inevitable orientation errors, wind drift, etc. (Mourit-
sen, 1998). Spatio-temporal programmes appear to be
inherited, and F1 hybrids show intermediate patterns
both temporally (duration of Zugunruhe; Berthold
and Querner, 1981; Berthold, 1988) and directionally
(Helbig, 1991, 1996; Berthold et al., 1992). Recently
these results obtained in lab tests in Emlen funnels
have been confirmed by tracking birds of hybrid origin
in the wild (Delmore and Irwin, 2014).
However, soon after E. Gwinner and W. Wiltschko
demonstrated that first-autumn garden warblers show
a preferred direction of spontaneous locomotor activ-
ity in round arenas corresponding to the migratory
direction in free-living conspecifics without external
information, on the basis of their inherited pro-
gramme alone (Gwinner and Wiltschko, 1978), Beck
and Wiltschko (1988) showed that juvenile pied fly-
catchers are not able to do that. The birds of the latter
species need the geomagnetic information corre-
sponding to their migratory route to successfully

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develop their innate spatio-temporal programme.
Later juvenile thrush nightingales (Luscinia luscinia)
from Sweden were shown to sharply increase their
fuelling rate if placed in the magnetic conditions of
northern Egypt, i.e., before a migratory flight across
the Sahara. The birds that remained in the magnetic
conditions of Sweden did not gain much fuel (Frans-
son et al., 2001). Importantly, these data refer to first-
autumn birds that had not yet experienced magnetic or
other conditions of Egypt.
It has been shown that first-autumn long-tailed tits
(Aegithalos caudatus) respond to decreasing day length
by increasing their locomotor activity, which in the
wild means a higher migratory speed in birds delayed
in northern areas (Bojarinova and Babushkina, 2015).
These and many other data suggest that apart from
clock (or calendar) and compass, naïve migrants have
some innate idea of the magnetic and/or photoperi-
odic conditions that they should experience during the
normal, according to schedule, movement along their
autumn migratory route, and can correct their migra-
tory behaviour if the schedule is not followed. It might
not be a full map, but rather a system of “beacons” or
“signposts” that allow first-autumn migrants to con-
trol their position on the migratory route. Satellite
tracks of juvenile birds, e.g. Eleonora falcons (Falco ele-
onorae) (Gschweng et al., 2008) and wandering alba-
trosses (Diomedea exulans) (Åkesson and Weimerskirch,
2014), are very difficult to explain by clock and com-
pass alone, without a map sense and at least some ele-
ments of an innate map.
In our opinion, sufficient evidence has been made
available to revise the clock-and-compass concept.
First-autumn migrants (possibly not of all species)
seem to be able to control their position to a varying
degree of accuracy on the basis of inherited informa-
tion. Which cues they use and the accuracy of their
control should be subjects of further studies. It is pos-
sible that in this respect, like in hierarchy of compass
systems, significant between-species variation will be
found, governed primarily by length and complexity of
migratory route. A chaffinch from the Baltic area
might be able to reach its species-specific wintering
area in southwestern Europe without an innate map,
whereas an Eleonora falcon hatched in the Mediterra-
nean may need such information to reach its non-
breeding quarters in Madagascar. It is even more diffi-
cult to imagine a Pacific golden plover (Pluvialis fulva)
breeding in Alaska and reaching its winter range in the
Hawaii without a map sense (Johnson et al., 1997).
The aforementioned considerations can be brief ly
summarised as follows. Migrating birds possess com-
pass systems that allow them to select and maintain
compass directions. At least three such systems are
currently known (solar, stellar and magnetic), even
though it cannot be ruled out that not all species and
populations are equally proficient in using all of them.
Details of each of these systems are not completely
clear and require further research, but their existence
is a rather well established fact. Hierarchy and interac-
tion of compass systems of migrants are poorly stud-
ied; quite possibly, avian species differ in this respect.
During migration birds learn how to use a map that
makes it possible to perform true navigation (i.e., to
detect their position in respect to the goal of migra-
tion) at the scale of their usual movements. The phys-
ical nature of the map is currently being actively stud-
ied; currently the most promising are the geomagnetic
and olfactory map hypotheses.
It is usually assumed that map is experience-based
and formed during migratory movements. This means
that the map exists only for the areas visited during the
life of an individuals, and possibly areas in their more
or less immediate vicinity. Migrating birds are believed
to have no innate map of the areas not visited earlier,
so that juveniles reach their species-specific wintering
areas for the first time by using their compass sense
and counting time, thus moving in a certain geneti-
cally inherited direction. However, in recent years evi-
dence becomes available that juveniles (possibly not of
all species of migrants) do have some mechanism
(possibly a crude one) of controlling their position on
migratory route, which allows them to compensate for
errors in their spatio-temporal programme to some
extent. This mechanism might be based on the param-
eters of the geomagnetic field.
Avian orientation and navigation research devel-
oped in the 1950s to early 1980s, after two main meth-
ods of behavioural experiments had been made avail-
able: lab tests in round arenas (Kramer, 1949) and
pigeon releases (homing; Matthews, 1951). Soviet
researchers participated in that research, in particular
in the studies of navigational map. An important study
that showed that in order to be able to return to their
natal area, migrating birds need to move across it (i.e.,
that they sample some physical gradients), was per-
formed on the Courish Spit by the members of the
Biological Station Rybachy of the Zoological Insti-
tute. Its results were published in 1984 in Zoologich-
eskii Zhurnal (Sokolov et al., 1984). In the late 1980s
and until the end of the 20th century, orientation
research declined somewhat, only to become more
active again since about 2000. The current phase is
characterised by an active collaboration between zool-
ogists, neurobiologists and biophysicists. Russian
researchers do participate in this development (Cher-
netsov et al., 2004, 2008, 2011; Kavokin, 2009;
Solov’yov et al., 2010; Kishkinev et al., 2010, 2013,
2015; Kavokin et al., 2014), but their contribution may
and should be more active.
ACKNOWLEDGMENTS
The author is sincerely grateful to A.L. Mukhin,
J.G. Bojarinova, L.V. Sokolov and an anonymous
reviewer whose comments contributed to improving

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ORIENTATION AND NAVIGATION OF MIGRATING BIRDS 799
earlier drafts. This study was performed with support
from Russian Foundation for Basic Research (15-04-
05386) and with participation of the Zoological Insti-
tute of Russian Academy of Sciences (01201351182).
The study has also been supported by St. Petersburg
State University (1.37.149.2014).
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