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54
Orientation and Navigation in the Animal World
Gillian Durieux and Miriam Liedvogel
Max Plank Institute for Evolutionary Biology, Germany
We often do not appreciate that the animals moving around
us in the background of our daily lives –the pigeons or
crows that fly past your window at work, for instance –
are not just moving around randomly or aimlessly. Like
us, they have places they want to go to and things they have
to do. An animal’s movement has purpose and can take it
accurately and precisely across both short and impressively
long distances; whether it is to find food, avoid predators,
search for mates, or, for some, to migrate across continents
to areas of higher productivity at certain times of the year.
Probably the most well-known examples of these large-
scale movements that require an impressively accurate
sense of direction are the seasonal long-distance return
migrations of birds to the same breeding and wintering
grounds year after year. Alaskan individuals of the north-
ern wheatear (Oenanthe oenanthe), for example, spend
the winter in sub-Saharan Africa, a return trip of around
29 000 km [1]. However, there are many other examples
from across taxonomical groups (Figure 54.1). Tracking
of humpback whales (Megaptera novaeangliae) on their
6500 km migration revealed that they swim in a straight,
constant direction for hundreds of kilometers while deflect-
ing only by less than 1 [2]. Similarly impressive feats are
found in fish [3, 4], insects [5, 6], and reptiles [7].
To accomplish directed movement, animals have to ori-
ent or navigate using the information presented to them
in their environments. For researchers who study how ani-
mals find their way around, orientation and navigation rep-
resent two different tasks [14, 15]. Orientation is the ability
to choose and follow a specific heading or direction, and is
commonly associated with the sole use of a compass system
to keep that vector [14, 15]. Navigation, on the other hand,
is a bit more complex. This requires an animal to work out
the relationship between its current location and its goal,
and then choose the correct course of movement based
on compass information to get there [14, 15]. When discuss-
ing navigation, researchers often use a map analogy to
reflect how we use a map as a reference to determine where
we are in relation to where we want to be [14, 15]. An ani-
mal that is displaced to a new location where it has never
been before would have to navigate to return to a known
area; that is, it has to use learned information from their
environment that will tell it where it currently is and then
pick the direction that will take it back [14, 15].
Orientation behavior with the combined use of a clock
and a biological compass is widely practiced in a huge array
of animals, both by naïve juveniles and experienced adults
[16, 17]. Navigation however, as it is the more complex of
the two, requires learning. To see this in action, one can
consider a classic experiment from the Dutch scientist, A.
C Perdeck, from the 1950s on starlings (Sturnus vulgaris),
which also nicely illustrates the differences between purely
innate orientation (by naïve juveniles on their first migra-
tory journey) and experience- and learning-based naviga-
tion [18]. Perdeck [18] ringed thousands of juvenile and
adult starlings as they were migrating through the Nether-
lands. He then displaced the birds to a new location and
released them. The results showed that juveniles continue
to head in a direction that they would have traveled in had
they not been displaced (a shifted parallel vector trajectory)
and so are using their compass to orientate as part of their
inherited set of migratory instructions (Box 54.1; [18]).
Adults, by contrast, realized their displacement and
adjusted their journeys accordingly, integrating learned
information that allows them to correct for the displace-
ment and head to their actual migratory destinations that
they had been to before [18]. In contrast to the inexperi-
enced juvenile birds on their first migratory journey that
used a vector orientation strategy, these adult birds were
therefore navigating and used a map [14, 18].
1689
Position, Navigation, and Timing Technologies in the 21st Century: Integrated Satellite Navigation, Sensor Systems, and Civil Applications, Volume 2,
First Edition. Edited by Y. T. Jade Morton, Frank van Diggelen, James J. Spilker Jr., and Bradford W. Parkinson.
© 2021 The Institute of Electrical and Electronics Engineers, Inc. Published 2021 by John Wiley & Sons, Inc.
54.1 What Information Do Animals
Use to Orientate and Navigate?
For animals, both orientation and navigation require
dependence on multiple sensory systems to detect sources
of directional information to use as a reference in their
environments. Some senses involved in these tasks are also
possessed by humans, such as olfaction or vision, but others
are entirely foreign to us such as the magnetic sense. Which
cues to use, in which combination and hierarchy, and when
to use them differ between taxa and species, and further
depend on how much resolution or detail they may require
at that particular time. This, of course, is also dependent on
which cues are available to the animal at that moment in
time. This can be best explained with reference to the dif-
ferent stages of a long-distance migratory journey.
Long-distance migration is thought to be a process invol-
ving several stages, with each stage demanding a different
level of accuracy or precision [26–28]. A fish on a mission to
return-navigate to a distant spawning site several thousand
kilometers away, for instance, may use information that
gives it a “crude,”rough directional heading toward its final
destination goal [27]. This is a long-distance orientation
stage [27, 28]. The fish would then require increasing
levels of accuracy for fine-tuning as it nears its goal,
requiring input from additional sensory systems, likely in
Figure 54.1 Examples illustrating the fascinating diversity and impressive scale of migratory journeys across various taxa. In red: Every
autumn, millions of monarch butterflies (Danaus plexippus) migrate thousands of kilometers from southern Canada and the eastern United
States to central Mexico, where they overwinter (Dingle et al. [8]). In spring, the monarchs will make their way north over successive
generations to begin the whole cycle again (Dingle et al. [8]) (Photo: Christine Merlin). In blue: Humpback whales (Megaptera novaeangliae)
which breed in Central America migrate 8 000 km or more to feed in waters off Antarctica (Rasmussen et al. [9]) (Photo: Kristin Rasmussen).
In orange: Loggerhead sea turtles (Caretta caretta) that hatch on the South Eastern coast of the United States migrate 12 000 km or more
along the North Atlantic gyre to seas around the Azores and back (Musick and Limpus [10]; Bolten et al. [11]) (Photo: Ken Lohmann) In
green: Willow warblers (Phylloscopus trochilus) from Denmark were tracked on their entire migration to their overwintering grounds in sub-
Saharan Africa –a remarkable feat for a bird that weighs less than 15 g (Lerche-Jørgensen et al. [12]) (Photo: Gernot Segelbacher) In purple:
The migratory journey of bar-tailed godwits (Limosa lapponica) can take some individuals from New Zealand to the Yellow Sea, to Alaska
and then back, clocking up around 29 000 km (Battley et al. [13]). From GPS tracks, we know that they can fly nonstop for a week or more
during some legs of this trip (Battley et al. [13]) (Photo: Phil Battley).
1690 54 Orientation and Navigation in the Animal World
combination, to continue to close in on its final goal [27,
28]. Finally, and presuming previous experience and
knowledge of the goal location, it could then rely on famil-
iar sea landmarks, or local cues to zero in on its goal [27].
This is a pinpointing stage [27, 28]. Long-distance
migration therefore proves to be a highly complex and
spatiotemporally coordinated phenomenon as animals
use combinations of different cues depending on their phys-
iology, the availability of reference cues, as well as the
required level of accuracy needed to master different legs
of their journeys [27, 28].
But what are these cues that allow the animal to master
these challenges and accomplish a successful orientation
task? We will highlight the different reference systems in
detail and illustrate the strategies animals may use to move
around their environments, by drawing on specific exam-
ples. As there are many other beautiful examples available
in the literature, we will point to reviews that summarize
and discuss these in more detail wherever possible for fur-
ther reading. You will realize that much of the focus is on
birds and insects. Historical and even contemporary orien-
tation and navigational research on vertebrates has cen-
tered on birds because they are iconic species well
known for their exceptional long-distance movements,
but we make an attempt to include examples from other
taxa wherever possible.
There are also technical advantages when working with
birds and insects. Insects are easier than vertebrates to rear
and keep in the laboratory, and testing them for their orien-
tation preferences under controlled conditions is again less
complicated than testing vertebrates. Migratory birds that
are kept in cages conveniently (for the researcher) exhibit
so-called Zugunruhe, or migratory restlessness‚once the
migratory season approaches. This characteristic behavior
is oriented and is characterized by high activity levels during
the night, including wing whirring, jumping, and flying
around in the cage; this is contrasted to the non-migratory
season, when birds typically sleep. Every spring and autumn
at night, birds would attempt to take off in the direction their
conspecifics migrate to in the wild [29]. In addition to orien-
tation, the captive migratory bird’s timing program for rest-
lessness activity is also in good accordance with the wild
migrants (e.g. [30]). When songbirds are contained during
Zugunruhe in a circular funnel-shaped cage lined with
scratch-sensitive paper, their preferred direction can be
measured by examining the scratches left on the paper as
the birds attempt to jump into the preferred direction in
order to take off [31]. This provides a useful way to measure
preferred directional heading in songbirds and allows
researchers to more easily test the response to various direc-
tional cues, for example, changing/manipulating the mag-
netic field vector as discussed later in this chapter [31].
54.1.1 Celestial Cues
Like human navigators for thousands of years when trav-
eling large distances, many animals look to the sky for
directional cues. At night and during the day, but also
at dusk and dawn, the sky and the celestial cues therein
can provide a wealth of information that can be used for
orientation.
Box 54.1 Genetic instructions and cultural transmission
The strategies by which animals migrate vary substan-
tially. Some animals migrate together in huge numbers.
These events can be spectacular, like the seasonal migra-
tion of hundreds of thousands of wildebeest in the
Serengeti as they follow grazing areas or the migration
of huge numbers of North America’s monarch butterflies
that sees several generations complete a migratory cycle.
Other animals like some species of geese and crane may
migrate in groups with family members, while other
species, like many night-migrating songbirds, migrate
entirely alone.
The animals that migrate successfully unaccompanied
and alone complete their first migratory journeys based
on inherited genetic instructions. This inherited program
directs all aspects of their migratory journey including the
timing, direction‚and distance (reviewed in [19]). In the
case of social species that travel in groups, their
navigational strategies may have to be learned or refined
by following others. Information that is transferred
between individuals during group navigation seems to
be especially important to naïve animals, which can learn
from more experienced individuals in their groups. Young
whooping cranes (Grus americana) for example, can learn
new overwinter sites or make their navigation more pre-
cise by learning from older birds in their group [20, 21],
and king penguin chicks (Aptenodytes patagonicus) find
their way back to their crèches more efficiently when
paired up with another chick with more experience
[22]. What is more, traveling together can offer distinct
navigational advantages over traveling alone for all indi-
viduals involved by enhancing the groups’collective nav-
igational accuracy (reviewed in [23]). For example,
homing pigeons home much more efficiently in pairs or
in small groups than when they home alone [24, 25].
54.1 What Information Do Animals Use to Orientate and Navigate? 1691
54.1.2 The Sun
During the day, the sun is a very prominent and highly vis-
ible reference point that follows a predictable and locally
stable trajectory in the sky. Every morning, it rises on the
eastern horizon and sets in the west, and so the position
of the sun relative to the horizon, the sun’s azimuth,
changes as the day progresses (Figure 54.2A). For diurnal
animals, this trajectory can act as a predictable directional
information source and can be used in a couple of differ-
ent ways.
The sun can be used to simply select an orientation direc-
tion and then keep a mean heading. This is the strategy
used by the painted lady butterfly (Vanessa cardui) to fly
southward in autumn on their migrations [32]. Alterna-
tively, some other animals adopt a more complex form of
this compass. Because the position of the sun gradually
changes throughout the course of the day, it is a moving
directional reference. Unless an animal can factor in this
movement of the sun, its chosen heading will slowly shift
along with the sun over the course of the day, inevitably
leading to inaccuracy and orientation error over longer dis-
tances [33]. Therefore, to accommodate the sun’s move-
ment, a more refined and accurate sun compass
combines information of the sun’s position with a form
of exact daily timekeeping. For animals, this clock comes
in the form of an internal circadian body clock, which keeps
roughly 24-hour rhythms [34, 35]. Briefly, in response to
environmental cues such as light and temperature, brain
structures interact to form approximate 24-hour patterns
in hormone secretions, generating night and day cycles
(reviewed by Refinetti [35]). By using the azimuth of the
sun in tandem with their circadian clock, animals can avoid
accumulating orientation errors [33]. This is known as the
time-compensated sun compass.
The litmus test for a time-compensated sun compass is
whether an animal shows a response in orientation behav-
ior to an experimental protocol called clock shifting. Clock
shifting offsets the animal’s circadian clock by forcing it to
adjust to an artificial light regime either several hours
behind or ahead of the real sun time [36]. Once the animal
has adapted to this altered light and dark cycle, researchers
can test the directional preference of these animals under
different light conditions and predict their resulting orien-
tation depending on their shifted subjective time regime.
For an animal to test positive for possession of a time-
compensated sun compass, it should deflect its orientation
direction by a predicable amount, because of the mismatch
between its circadian clock and the sun’s position [36]. This
is equivalent to approximately 15 of deflection in direction
per hour of clock shift [36]. If the animal’s orientation direc-
tion is unaffected by clock shifting it implies that its sun
compass is not time-compensated. Ideally, this should be
tested for in the absence of other directional cues so that
an animal cannot access other types of information to
orientate.
Clock shifting has revealed that a taxonomically diverse
group of animals make use of a sophisticated time-
compensated azimuth sun compass, including insects
[37], birds (reviewed by Schmidt-Koenig et al. [36]), fish
[38], reptiles [39, 40], mammals [41], and amphibians [42].
azimuth angle
path of sun
AB
NN
Figure 54.2 ASchematic of the path of the sun through the sky. In the Northern Hemisphere‚the sun’s arc is in the southern part of the
sky. The azimuth is the angle of the sun along the horizon described as the degrees from geographic North. BThe polarization pattern of
the sky is represented by dotted lines. The thickness of the lines mirrors the degree of polarization; the thicker the lines, the higher the
polarization. Polarization from the sun’s position increases with distance away from the sun, reaching a maximum at 90 from the sun
before it decreases again.
1692 54 Orientation and Navigation in the Animal World
The best-understood time-compensated sun compass is
that of the monarch butterfly (Danaus plexippus) [43]. In
monarchs, the time-compensated sun compass is the chief
orientation mechanism used to complete their multi-
generational migrations; they use it to select a southerly
direction from North America and Canada to Mexico in
autumn and then again use it to move northward in spring
[37, 44–46]. In overcast conditions, monarchs seem to be
able to take advantage of the magnetic field for directional
information as well ([47]; but see [44]). The monarch circa-
dian clock used in the sun compass is located in the anten-
nae [43]. This was confirmed with removal of the antennae,
which left monarchs disorientated and unable to use their
sun compass [43]. When researchers prevented light from
reaching the circadian clocks in the antennae by painting
them with black paint (disabling the ability of butterflies
to maintain a rhythmic body clock), the butterflies showed
a different flight orientation than butterflies with uncov-
ered antennae [43]. It was further shown that monarchs
integrate clock information from their antennae to work
as part of the sun compass [48]. This was cleverly demon-
strated by a series of experiments carried out by Guerra
et al. [48], who found that butterflies orientate perfectly
well with only one intact antenna (and the other one cut)
[48]. Just a single antenna was enough to synchronize
the internal clock and allow for directed flight [48]. By
contrast, painting just one antenna black instead of cutting
it, while leaving the other antenna intact, resulted in
de-synchronized clock information and disoriented flight
[48]. This showed that conflicting clock information com-
ing from both antennae (one painted black and one
untouched) to the brain disrupts the sun compass [48].
The final confirmation of this was obtained when the
researchers removed the painted antenna that caused the
confusion —this enabled the butterflies to recover and
use their sun compass perfectly [48].
In birds, the sun compass has been studied in migratory
birds as a reference cue during migration [49] and in hom-
ing pigeons (Columba livia) during homing [50–52]. Gustav
Kramer equipped orientation cages with horizontal win-
dows allowing for a view of the sun’s position and could
show that European starlings (Sturnus vulgaris) were able
to maintain their heading throughout the day to orientate
toward food goals [49], demonstrating the use of a time-
compensated sun compass. To what extent the sun compass
is used in day-migrating birds during actual migration in
the wild is still a matter of debate, and results of clock-
shifting experiments are not entirely conclusive [53–56].
Very recently, clock shifting was applied to a free-flying
bird, the Manx shearwater (Puffinus puffinus), and these
results suggest that they use time-compensated solar infor-
mation to find their way back to their colonies [57].
54.1.3 Polarized Light
Many animals have the ability to detect polarized light, and
representatives have been found from most animal groups,
including fish, reptiles, birds‚and many species of inverte-
brate (reviewed by Horváth [58]). For many of these organ-
isms, the clear patterns of linearly polarized light in the sky
that follow the course of the sun can be used as a compass
cue to orient and navigate [Box 54.2]. Due to the morpho-
logical architecture of their compound eye, insects are par-
ticularly adept at detecting polarized light and using it to
orientate, so the following subsection will largely focus
on insects and their activities.
The first evidence of an animal taking advantage of polar-
ized skylight for compass orientation came from experi-
ments on honeybees by Karl Von Frisch [59]. It was
subsequently demonstrated that honeybees are still able
to use directional information from the sun when it is
obscured or out of view, and this is accomplished by per-
ceiving polarized light patterns in clear patches of sky
[60, 61]. Bees use this information when out foraging,
and upon return to the hive, they share information about
food sources with their siblings [59–63]. This information is
encoded in their “waggle dance”and contains both the dis-
tance and the direction from the hive to the food location
[62] (this is a form of path integration, previously discussed
Chapter 53).
It was further demonstrated that polarized skylight also
provides a directional reference for the path integration tac-
tics of foraging desert ants of the genus Cataglyphis [64–66].
Found in arid, hot, and barren regions like deserts, often
Box 54.2 The polarized sky
Light is an electromagnetic wave and is described as
polarized or unpolarized based on how its electric field
vibrates. When the electric field vibrates in all directions
along its travel direction, it is described as unpolarized
light. When the electric field vibrates in one direction, it
is known as linearly polarized light. The sun’s light is
unpolarized, but as it travels through the atmosphere it
is scattered by atmospheric particles, linearly polarizing
the light. This is known as Rayleigh scattering and creates
a pattern of linearly polarized light in the sky following
the sun that animals can use as a directional reference
(Figure 54.2B).
54.1 What Information Do Animals Use to Orientate and Navigate? 1693
devoid of any landmarks, they run out momentarily in the
hot sun to forage on insects that have died of heat exhaus-
tion [67]. Their outbound food searches can take them in
long, circuitous routes across the hot sand, at times cover-
ing more than 100 m [68]. Yet as they make their searches,
they keep track of their steps with an internal mechanism
that can be compared to a pedometer, and they are also
aware of their direction based on celestial cues like polar-
ized light [66, 68, 69]. This means that once they have
located a food item, they hurry back in an impressively
straight line right back to their nest [68]. It is an elegant
and sophisticated mechanism that allows them to survive
in their extreme environments.
It is not just diurnal insects that can use polarized light to
orientate themselves. Nocturnal ants, like nocturnal bull
ants (Myrmecia sp.) that are active during astronomical twi-
light hours, have also been found to use the polarization
patterns of the sun as it sets to orientate themselves on fora-
ging trips [70, 71]. Remarkably, some insects have such sen-
sitive vision that they can also take advantage of the
polarization patterns of moonlight in the night sky to orien-
tate [72, 73]. The dung beetle (Scarabaeus zambesianus)
uses the sun’s polarized light patterns during twilight to roll
its freshly made dung ball in a straight line away from the
dung pile [74]. When the sun is far beyond the horizon,
however, it can detect and use the moon’s polarized light
patterns as a compass despite polarized moonlight being
a million times more faint than that of the sun [72].
Investigation of insects’compound eyes such as ants and
crickets has revealed that insects sense polarized light from
sensors located at the top of their eyes, called the dorsal rim
area [75, 76].
In insect eyes, photoreceptor cells contain structures
called rhabdomeres [75, 77]. Each rhabdomere has a lot
of finger-like projections of its membrane called microvilli,
which maximize the rhabdomere’s area, and these are
packed full of visual pigment molecules [75, 77]. Visual pig-
ment molecules should be aligned to each other to enable
polarized light sensing [75, 77]. In the dorsal rim area, the
microvilli “fingers”of the rhabdomeres lie parallel to each
other, also arranging the visual pigment molecules in align-
ment with each other [75, 77]. It is this feature that is
important in making the dorsal rim photoreceptors sensi-
tive to specific polarized light directions [75, 77].
Polarized light sensitivity has also been detected in some
vertebrate groups (reviewed by Horváth et al. [78]).
Research has shown that migratory songbirds use polarized
light cues to calibrate their compasses such as their mag-
netic compass (discussed below) at sunset [79–82] reviewed
and discussed in [83]. A couple of behavioral studies have
also supported orientation by polarized light in bats [84,
85]. Greater mouse-eared bats (Myotis myotis) were found
to use polarized light to calibrate their magnetic compass
in a similar way as migratory birds [84, 85]. However, the
sensory mechanism underlying polarized light sensitivity
in vertebrates remains rather mysterious [83].
It is worth noting that there is one mammal that can def-
initely detect polarized light. We humans can see it as well –
something that may come as a surprise to many [86]. Some
individuals, when looking at highly linearly polarized light,
will see two bowtie shapes stacked on top of each other
imposed on the center of their visual field (discussed in
more detail in McGregor et al. [86]). There is a yellow shape
oriented perpendicular to the polarization‚and the blue is
parallel to the polarization. This effect is known as the Hai-
dinger’s brush, and they may be seen in the clear, sunny sky
[86]. It can also be detected when looking at a white back-
ground on an LED computer screen. It is thought that the
phenomenon is generated by carotenoid pigment mole-
cules in the macula (an area of the retina) (review by
McGregor et al. [86]). This effect has led to some interesting
speculations about the navigation of historic populations of
Vikings [78].
54.2 Star Compass
Most songbird species choose to migrate at night. Nocturnal
migration makes them less likely to be blown off course
because the weather is generally less tumultuous, the tem-
peratures are cooler, and they are less prone to being pre-
dated at this time [87, 88]. To successfully master these
long-distance travels, songbirds must be using cues availa-
ble at night to guide them on their journeys. Starting in the
late 1950s, researchers began to test whether birds use the
stars to find their way. Planetariums proved to be the ideal
setting for these experiments as they allowed researchers to
manipulate the star patterns and star movement above
birds placed in circular orientation cages in a controlled
manner. In this way, researchers showed that a variety of
bird species do indeed have the ability to extract directional
information from the starry sky [89–91].
Because Earth turns on its axis, for an observer on Earth,
the stars appear to move in circular tracks through the sky,
and the center of this rotation points poleward. In the
Northern Hemisphere, Polaris, also called the North Star,
sits at the heart of this rotation. Studies find that when birds
hatch, they instinctively look at the stars and through a
learning period of a couple of weeks judge the poleward
direction by finding the point in the sky around which
all the other stars appear to be rotating around
(Figure 54.3A) [89–93]. When they go through this prelim-
inary learning stage, it appears that they are purely seeking
1694 54 Orientation and Navigation in the Animal World
out the center of star rotation, and other specific celestial
features such as constellations or individual stars are unim-
portant [90–94]. In the planetarium, for example, any other
arbitrary region in the sky can be the center of rotation,
whether there is a star in the center or not, and juvenile
birds will accept the rotational center as their reference
cue for poleward direction [90–92]. This will even work
with an entirely simplified, artificial “starry sky”as
Wiltschko and colleagues [94] found when young birds
learned to use 16 rotating artificial light points as reference
for a star compass.
As they grow older, it appears that birds judge which way
is poleward from just looking at the star constellations and
no longer need to take time to judge the rotation center of
the stars’rotational movement [90–93]. By their first migra-
tion therefore, it has developed into a sharpened, more effi-
cient compass mechanism.
In general, star compass use in animals has not received a
considerable amount of attention compared to other com-
pass systems, maybe due to experimental and logistical con-
straints. Although more recently, the extent to which star
cues may help dung beetles keep a straight bearing while
they roll their dung balls was tested in a planetarium
[95]. Dung beetles (Scarabaeus satyrus) do not orient using
individual stars [95], but rather use the starry band of the
Milky Way to keep rolling in straight lines [95]
(Figure 54.3B). Moreover, a few tantalizing studies show
that even some marine mammals may use a star compass
to orient. Harbor seals (Phoca vitulina) can see bright stars
in the sky and were trained in a planetarium to be able to
search out the star Sirius and touch their noses to its
azimuth with accuracy [96, 97]. This suggests that they
have the sensory capabilities for at least identifying specific
stars, patterns, or the rotational center, and hypothetically
could keep a bearing with them [96, 97]. It has been specu-
lated that whales and dolphins may be looking for cues to
orientate when they lift themselves out of the water (spy
hopping behavior), but whether they or other marine mam-
mals have the similar capabilities as harbor seals remains to
be proved [97].
Currently, it is not understood how animals like birds
identify the rotational center of the stars. Tracking the lit-
eral “movement”of the stars would require animals to be
able to see incredibly slow-moving rotations –the stars
rotate at a speed of around 0.0042 degrees per second
(/s). Behavioral tests imply that it is rather unlikely they
detect these extremely slow motion traces. This has been
specifically tested in pigeons very recently‚suggesting that
pigeons are not able to detect slow-moving rotational dot
patterns at this speed [98]. Similarly, the general motion
sensitivity ranges in other animal taxa suggest that animals
are likely able to distinguish objects at higher speed ranges.
It seems that their comfortable lower thresholds are gener-
ally still a fair degree higher than what would be required to
detect celestial motion. For example, rats and mice have a
comfortable motion sensitivity of around 20–80 /s [99], and
the Jacky dragon lizard (Amphibolurus muricatus)ismore
comfortable above 10 /s [100]. Humans seem to be much
more sensitive to motion than pigeons, rats, and mice
[99, 101] (and obviously from our own life experience we
can say we cannot see the stars literally move). Although
these sensitivity tests in other taxa are not studied from
AB
Figure 54.3 ABirds use the rotational center of the stars to infer a poleward direction (Emlen [90, 92]). This schematic depicts the
scenario for the Northern Hemisphere, where the star Polaris lies nearly exactly in the center of the celestial rotation and thus appears
stationary. BThe dung beetle does not orient using specific star patterns to keep a straight heading (Dacke et al. [95]). Instead, it uses the
band of light from the Milky Way as a reference to keep a straight line (Dacke et al. [95]). Source: Reproduced with permission of Elsevier.
54.2 Star Compass 1695
the perspective of orientation or navigation, we assume it is
not too daring to extrapolate that generally, animals are
more sensitive to moving objects at speeds that are several
orders of magnitude higher than the rotation of the starry
sky. Should a rotation-based star compass be confirmed in
other animals too, it would seem rather unlikely to work on
the basis of directly seeing celestial rotational motion.
Another strategy that could circumvent this motion sensi-
tivity issue could involve the use and integration of snap-
shot images that compare the position of the stars over
time with a snapshot memory of the stars’previous position
perhaps in relation to landmarks [28, 98]. Foster et al. [102]
present an excellent review discussing the starry sky in light
of orientation and navigation.
54.2.1 Olfaction
Olfaction is biologically universal; all animals have the abil-
ity to sense odors or chemicals in their environment [103].
Although olfaction is a sense we humans share with other
animal taxa, in most contexts we attach less importance to
it [104]. This is also the case when it comes to using olfac-
tion as a reference cue when moving around space. In con-
trast to humans, many other animals do depend
significantly on olfactory cues for orientation and naviga-
tion. Given our comparatively limited sense of smell, it
may seem inconceivable that an animal could be relying
on olfactory cues to travel across long distances on migra-
tions or use olfactory gradients as guidance on long fora-
ging trips. But as we will outline and discuss in the
following, many species certainly do so.
For many pelagic marine animals, chemical or olfactory
cues can present orientation cues in landscapes almost
devoid of any distinct visual features. These cues can be rel-
evant for orientation even across large areas of open ocean
during long-distance foraging trips. In this environment,
tasks such as searching for areas of food (the distribution
of which can often vary both spatially and temporally) can-
not be carried out indiscriminately, and reference cues are
needed for directed movement [105].
One order of seabirds, the tube-nosed Procellariiformes,
comprising albatrosses, petrels, fulmars, and shearwaters,
can spend weeks at a time ranging across hundreds of kilo-
meters of open ocean [105]. They feed on fish, squid, and
krill, and trying to find these in vast stretches of open ocean
can seem like a needle in a haystack scenario [105]. Tube-
nosed seabirds are gifted with an extremely well-developed
sense of smell, and the brain regions that are responsible for
smell in these species are huge –up to a third of their brains
may be dedicated to the sense of smell [106, 107]. In com-
parison, in the house sparrow (Passer domesticus) brain,
approximately 4% is dedicated to olfaction [106, 108]. Olfac-
tion plays an important role in the lifestyle of Procellarii-
formes, and it is thought that to find areas where their
prey is likely to be, these birds largely use their keen sense
of smell (reviewed by Nevitt [107]). Procellariiformes seem
to be very sensitive to specific gases including dimethyl sul-
fide (DMS) [109, 110]. DMS release is triggered when zoo-
plankton grazes on phytoplankton [111]. The zooplankton
fall prey to other species, which in turn provide a feeding
base for animals higher up the trophic level [105, 112]. This
gas therefore is a marker for nutrient- and species-rich
areas with an assortment of animals such as fish, squid,
and krill feeding and grazing, which provide food for sea-
birds [105, 112]. It is thought that by following traces of
DMS when on the wing, seabirds can source out and orient
to potential food locations (reviewed by Nevitt [107]).
The specific sensitivity to DMS is not exclusive to the Pro-
cellariiformes. It appears to be present in a wide variety of
animals such as harbor seals (Phoca vitulina) [113], pen-
guins [114, 115], turtles [116], sharks [117], adult reef fish
[118], and more recently, reef fish larvae, who also may use
DMS cues, among others such as acoustic cues, to detect the
right reef habitat to settle [119, 120]. Using DMS as a cue for
orientation, therefore, may be an adaptation that is very
widespread and common in marine animals.
But can animals form a map with olfactory cues and use it
for long-distance navigation? And if so, to what degree are
olfactory cues used in an animal’s mapping of their envi-
ronment? These are questions that still remain controver-
sially discussed in the scientific community [121].
Olfactory maps have mainly been studied in the context of
pigeon homing (reviewed by Gagliardo [121]). It was found
that pigeons with their sense of smell disabled struggle to find
their way back to their home aviary when they are released
from a location new to them [122, 123]. When pigeons with
a functioning sense of smell are shielded from the winds
around their home aviary, they also fare badly at the same nav-
igation task [124]. Presumably, this blocks their access to odors
caught on the wind and prevents them from being able to con-
struct an olfactory map, and so they cannot find their way back
home from a novel location. And lastly, pigeons can be
“fooled”when you manipulate the direction in which olfac-
torycuesarepresented;when researchers shiftedthedirection
in which odors were presented by 180 , the pigeons responded
with an appropriate shift in their heading [125, 126]. Pigeons
can also learn to use artificial odors such as olive oil and tur-
pentine as navigational cues [127].
More recently, evidence for olfactory navigation is not
restricted to work on homing pigeons, and research on wild
birds is becoming more substantial. The Procellariiformes
sense of smell has been found to play a substantial role
1696 54 Orientation and Navigation in the Animal World
in true navigation even over large distances in these species
[128]. Displacement experiments on shearwaters (Calonec-
tris sp.), for example, have shown that these birds rely more
on their sense of smell rather than the geomagnetic field to
find their way back to their colonies hundreds of kilometers
away [129–131].
There is some evidence that this is the case for other taxa,
too. Sharks may need olfactory cues for navigational tasks
[132, 133]. Pelagic leopard sharks (Triakis semifasciata) that
had their sense of smell temporarily disabled had more
trouble finding the coast after being relocated to an unfa-
miliar area 9 km away than sharks that had a functioning
sense of smell [132]. Similarly, young blacktip reef sharks
(Carcharhinus limbatus) were much more efficient at cor-
recting for an 8 km displacement when they could use their
olfactory sense than reef sharks with their olfactory sensing
disabled [133].
For some species, their sense of smell also appears to be
vital for navigation during migration. One of the best-
established uses of olfactory cues in vertebrates is in the
natal homing of salmonid fishes. Salmonids begin their
lives in freshwater streams where they can remain for
up to a year or longer [134, 135]. Then the fish embark
on their seaward migration, and they can spend several
years at sea feeding until they reach sexual maturity
[134, 135]. This prompts their migratory return to their
freshwater natal streams to spawn [134, 135]. This can
be an impressive undertaking, and some salmon can swim
over 3000 km upstream against the current [134]. It is
thought that to begin with, during the open ocean phase
of their journey, they use a variety of information to find
their way to the coast, including information from the geo-
magnetic field [136, 137]. Then, once at the mouth of the
river, they switch to focusing chiefly on olfactory cues to
make their way to the streams where they were born
(reviewed by Bett and Hinch [137]). The mechanism by
which they do this is olfactory imprinting; when they were
juveniles they learned the chemical composition of their
natal waters (reviewed by Bett and Hinch [137]). As adults
they then follow these chemical cues to find the spawning
grounds on their migratory journey (reviewed by Bett and
Hinch [137]).
More recently, researchers believe that for some species
of birds, olfactory cues are also important for a successful
migratory journey. Wikelski and colleagues [138] showed
that lesser black-backed gulls (Larus fuscus fuscus) need
their sense of smell to find their way back to their migratory
corridor to get back on their migration track after a dis-
placement of around 1000 km. Tests on catbirds (Dumetella
carolinensis) revealed that the olfactory sense is also impor-
tant for their migratory navigation [139].
54.2.2 The Geomagnetic Field
The geomagnetic field has been present for most of Earth’s
history, with the earliest, concrete evidence of its existence
dating back at least some 3.5 billion years [140, 141].
Roughly coinciding with this time are the first signs of life
–microfossils of microbial ecosystems in rocks from Aus-
tralia and Greenland [142, 143]. So it is fair to say that
the magnetic field has been pretty much omnipresent for
life on Earth, with life having established itself on what
is essentially a giant electric field generator. In this light,
it is perhaps not so unexpected that many organisms have
taken to exploiting this persistent (being available through-
out the whole day and in overcast conditions) information
source as a directional resource, much like humans have
with our technological devices.
The 1960s marked the inception of research into mag-
netic sensing or magnetoreception in animals. Songbirds
provided a good starting point, known for their exceptional
long-distance movements, which require outstanding nav-
igational skills. Night-migratory songbirds are further well
suited for behavioral tests, because their nocturnal orien-
tated movements during the migratory season (migratory
restlessness or Zugunruhe as described earlier) can easily
be quantified in the laboratory under controlled conditions.
Taking advantage of this behavior, Merkel and Wiltschko
[144] tested European robins (Erithacus rubecula) in funnel
cages placed in the center of a magnetic Helmholtz coil sys-
tem. With these giant coil systems (diameters up to 2 m),
researchers can create a uniform magnetic field around
the test animal that can be readily manipulated to test var-
ious conditions concerning the magnetic sense. For exam-
ple, intensity values can be altered, or the direction of the
resulting field vector can be shifted in any dimension, per-
mitting researchers to check for the resulting change in ori-
entation behavior. In their study, Merkel and Wiltschko
could show that shifting magnetic north to point toward
geographical West or East caused European robins to adjust
their orientation preference accordingly, providing the first
substantial confirmation of an animal using Earth’s mag-
netic fields to extract directional information for orienta-
tion [144].
Knowing that Earth’s magnetic field is used for compass
orientation during migration, researchers were curious to
understand what features of Earth’s magnetic field were
birds actually using as a cue? There are various aspects of
the geomagnetic field that differ across the globe, which
could hypothetically provide directional information
(Figure 54.4). First, the magnetic field has a north and south
magnetic pole. An animal could hypothetically sense this
polarity and get a sense of north or south, similar to the
functioning of our magnetic compass needle reliably
54.2 Star Compass 1697
pointing toward north. The intensity of the magnetic field
also shows spatial differences, with the highest values at the
magnetic poles and substantially lower values as you move
toward the equator, where the lowest intensity values are
found. This difference in intensity could provide an indica-
tion of direction to an animal. Furthermore, the magnetic
field inclination angle or magnetic dip (here defined as
the angle at which the magnetic field lines meet Earth’s sur-
face) also differs across the globe; it is steepest (perpendic-
ular to the surface) at the poles and becomes shallower as
you move toward the magnetic equator, where the field
lines run parallel to Earth’s surface. The magnetic field vec-
tor points up in the Northern Hemisphere and down in the
Southern Hemisphere, and the inclination angle is horizon-
tal at the equator.
To see which of these features are used by the animal to
detect directional information, Wiltschko and Wiltschko
[146] altered different components of the magnetic field
vector and tested European robins for their behavioral
response. When they shifted just the polarity of the mag-
netic field (without altering the inclination angle) by flip-
ping both the vertical and horizontal component of the
magnetic field vector, they found that the birds’behavior
remained unchanged –the birds continued to orient into
their natural migratory direction, which is toward north
in the spring (Figure 54.5A). When either the horizontal
(Figure 54.5B) or the vertical (Figure 54.5C) component
of the field vector alone was flipped, resulting in a change
in inclination angle compared to the natural field vector,
the orientation heading of the birds reversed in the opposite
direction. Birds were now orienting toward geographical
south, which in the scenario of Figure 54.5B corresponds
to magnetic south, though in Figure 5C magnetic north
and geographical south coincide. This was a clear indica-
tion that the magnetic compass of birds does not function
like our magnetic ship compass, which is polarity based.
In fact, birds cannot distinguish between north and south,
but instead they detect the inclination of the magnetic field
(highlighted in orange in Figure 54.5) and only respond to
changes in the inclination angle, using this as a reference
cue to identify poleward (the inclination angle becoming
steeper) and equatorward (the inclination angle becoming
smaller) [146]. It was also found that the bird’s magnetic
compass only works within a specific intensity range, tuned
to the local magnetic field [147–149]. However, birds are
able to reestablish themselves when they are given some
time to adapt and adjust to different intensities that fall out-
side this known local intensity range [147–149].
Magnetic compass use was subsequently confirmed in a
range of bird species and other animals like reptiles, amphi-
bians, mammals, fish, and invertebrates (reviewed by
Wiltschko and Wiltschko [150]). It is now recognized that
S
N
magnetic
South
Magnetic
equator
magnetic
North
∼ 60.000 nT
∼ 30.000 nT
∼ 60.000 nT
intensity
intensity
Figure 54.4 Schematic of Earth’s geomagnetic field, which in essence resembles a giant bar magnet with field lines leaving Earth’s
surface at the South Pole, curving around the planet and re-entering Earth at the North Pole. The magnetic field vector points upward on
the Southern Hemisphere and downward on the Northern Hemisphere, and inclination angles are steepest at the poles and horizontal to
Earth’s surface at the magnetic equator. Intensity values vary depending on the location on Earth, with the highest values (60 000 nT) at the
poles and lowest values (~30 000 nT) at the magnetic equator (Modified from Wiltschko and Wiltschko [145]). Source: Reproduced with
permission of Biologists.
1698 54 Orientation and Navigation in the Animal World
magnetoreception is a trait that is present in a huge variety
of animals from all major taxa and not limited to migratory
animals (e.g. chicken: Freire et al. [151], zebra finch: Keary
et al. [152], and mice: Muheim et al. [153]), a club which we
are apparently not a part of (but see [154]). The magnetic
inclination compass also forms part of the compass reper-
toires of monarch butterflies and sea turtles, which they
use to orient on migration [47, 155]. The type of magnetic
information that animals use as a directional reference can
differ between taxa, and not all animals tested have an incli-
nation compass. Other than birds, some animals such as
mole rats (Cryptomys spp.), bats, and spiny lobsters (Panu-
lirus argus) [156–159] seem to use the polarity of the mag-
netic field and not the inclination angle as a reference cue
for orientation.
Once it was confirmed that a wide array of animals do
indeed use the magnetic field as a compass cue for orienta-
tion, researchers began to consider whether the informa-
tion could also be used for the purpose of a positional
map or signpost sense [160]. For several species from a
range of taxa, the use of the magnetic field as part of a
map system could be confirmed [161–166]. It is thought
that birds use magnetic information both as a compass as
well as a map reference during migrations. Support for this
comes from a simulated magnetic displacement study on a
small songbird. Eurasian reed warblers (Acrocephalus scir-
paceus) were caught during their spring migration and
exposed to a magnetic field that imitated a displacement
1000 km eastward from their current location [165]. This
new magnetic field information did indeed make the war-
blers think that they were geographically displaced to a dif-
ferent location‚and they attempted to correct for it by
orientating in a way that would have taken them back to
their initial goal –their breeding grounds [165]. Because
nothing else but the magnetic field was altered, these
results clearly show that reed warblers use the ambient
magnetic field properties as a map reference to determine
their position in space [165].
A
N/S
SNNS
S/N N
?
S
Polewards
Polewards
Polewards
B
CD
Figure 54.5 Birds use a magnetic inclination compass. Depicted is the scenario of a European robin during spring, migrating northward
toward its breeding grounds. Blue lines represent the magnetic field vector (dashed lines indicate the vertical and horizontal component of
this resulting vector), and the directions of the arrows show the polarity of the field lines. Birds use the inclination angle (i.e. the angle at
which the magnetic field meets Earth) as a reference cue for magnetic compass orientation. AThe directional preferences of the bird do not
change when the polarity is reversed (i.e. horizontal and vertical vector flipped). BFlipping only the vertical component of the field vector,
resulting in a changed inclination of the magnetic field, causes the bird to orientate in the opposite direction, changing its heading by 180
and now migrating to geographic south (coinciding with the manipulated magnetic north). CHere only the horizontal component of the
magnetic field vector is reversed, resulting in a similar scenario as in B (the inclination remains the same), but polarity of the magnetic field
is reversed. Scenarios in Band Clead to the same behavioral orientation direction, clearly indicating that polarity is not used for magnetic
compass orientation. DBirds are disorientated when the inclination of the magnetic field is horizontal, which provides ambiguous
information and no clear directional reference (modified after Wiltschko and Wiltschko [146]). Source: Reproduced with permission
of AAAS.
54.2 Star Compass 1699
A magnetic map sense has also been found in sea turtles
using the same simulated displacement experimental setup
[167]. Sea turtles tend to be highly faithful to specific feed-
ing, overwintering, or nesting grounds, returning year after
year to the same sites, and can travel hundreds to thousands
of kilometers across featureless ocean between these loca-
tions [168, 169]. This fidelity to precise locations indicates
that they have refined navigational abilities, making use of
some type of map [167]. To test whether sea turtles can use
the magnetic field to extract positional information to form
part of a map sense to guide them on these journeys, Loh-
mann and colleagues [167] caught green sea turtles (Chelo-
nia mydas) in Florida and tested them in an artificial
simulated magnetic displacement study close to their catch-
ing grounds. The turtles were split into two experimental
groups: one group experienced a magnetic field that mim-
icked a magnetic field that was 337 km north of where they
were caught‚and the other group was tested under a mag-
netic field that mimicked a magnetic field 337 km south of
the catch area [167]. The turtles in both groups orientated
in a way that would have taken them back to the location
where they were caught, with the group that got the north-
ern magnetic field orientating south and the other group
vice versa [167]. This experiment showed that turtles can
determine their position in relation to their goal using
information provided by the ambient magnetic field and
use it to navigate. Interestingly, turtles do not even have
to learn how to use this information, but seem to be born
with an innate magnetic map sense (reviewed by Lohmann
et al. [170]). Turtle hatchlings that have never migrated
before will orientate in the direction that would keep them
on track with their migratory route when exposed to mag-
netic fields from varying locations (reviewed by Lohmann
et al. [170]). Thus, they have an inherited response to spe-
cific magnetic fields or “navigational markers”(reviewed
by Lohmann et al. [170] and Putman et al. [171]).
This inherited response to orient in an ecologically rele-
vant direction after exposure to simulated magnetic fields
mimicking the magnetic makeup of specific geographical
locations was also shown to be present in other animals.
Migratory-naïve juvenile salmon (Oncorhynchus tsha-
wytscha) and also juvenile glass eels (Anguilla anguilla)
[136, 172], amphibians [173, 174], and spiny lobsters
[164] have been shown to possess an inherited magnetic
map sense. The spiny lobster so far remains the only inver-
tebrate with the demonstrated capacity to extract positional
information for navigation based on magnetic cues.
54.2.3 Mechanisms to Sense Magnetic Fields
Knowing that animals use Earth’s magnetic field for orien-
tation and having identified the key characteristics of the
magnetic field that animal’s exploit as an orientation
reference, we want to understand how exactly animals
sense the magnetic field. Despite decades of work, this
question still remains to be answered. This has been a dif-
ficult task, not least because this sense is so far removed
from our own sensory experiences, but also because the
magnetic field passes through all biological material, so it
is difficult to pinpoint a sensor in the body. However, the
characteristics of the magnetic field that animals use to ori-
entate that we have identified based on behavioral experi-
ments provide us with clues as to what sensory organs
might be involved in the reception process. Most of the
work on identifying the magnetoreceptor, especially in
the last decade, has almost exclusively focused on birds.
Based on birds, two potential mechanisms have been put
forward: (i) a chemical reaction in the bird’s eyes known
as the radical-pair compass, and (ii) a mechanical receptor
based on magnetic particles.
54.3 Radical-Pair-Based
Magnetoreceptor
The radical-pair mechanism has been suggested to possess
the chemical properties needed to function as a magnetosen-
sor [175, 176]. It is based on light-induced radical pairs that
are generated upon photoexcitation within suggested recep-
tor molecules. In fact, behavioral experiments in insects,
amphibians, and birds suggest that the magnetic compass
is dependent on the presence of light of specific wavelengths
and intensities [177–182]. This led to the conclusion that the
magnetic compass was indeed a light-dependent mechan-
ism. Currently, the only known candidate molecules present
in the vertebrate eye that are equipped with the necessary
spin chemical prerequisites to act as such a magnetosensor
are cryptochromes, photosensitive molecules that are usu-
ally discussed in their role as regulators of the molecular
machinery of the circadian clock [176, 183]. To function
as a magnetoreceptor, light would trigger the formation of
a transient radical pair that results in different yields of
chemical end products, depending on the molecule’s orien-
tation within the magnetic field (very simplified after Ritz
et al. [176]). It would require a specific array of receptor
molecules, so that an animal could compare the products
of the light-sensitive reactions in various directions. Hore
and Mouritsen [184] provide a wonderful, more comprehen-
sive review of the radical-pair mechanism.
54.3.1 Magnetite-Based Magnetoreceptors
An alternatively hypothesized magnetoreceptor mechan-
ism may function by the force produced when magnetic
particles located somewhere in the body respond to Earth’s
magnetic field [185, 186]. This force is much like the
1700 54 Orientation and Navigation in the Animal World
pressure a magnet would exert in your hand when trying to
align with the field of another magnet. These nanoparticles
could be crystals of magnetite or maghemite, iron-sulfide
magnetic mineral [185, 186]. To form a functional receptor
system, these crystals could, for example, be anchored to
the plasma membrane of specialized receptors or ion chan-
nels, which open and close based on the force of this parti-
cle’s response to the magnetic field [187–189]. There are
multiple ways in which magnetite crystal could hypotheti-
cally be interacting with ion channels, and Cadiou and
McNaughton [189] provide a useful discussion of these
and more details on the mechanistic properties. For a mag-
netite-based system to be a feasible magnetoreceptor, the
crystals need to fall into a specific size range so that they
have a single magnetic domain (reviewed by Cadiou and
McNaughton [189]).
What type of mechanism an animal has or uses seems to
vary between animals and also with the purpose, and it is
possible that different reception mechanisms act comple-
mentarily and in concert. There is also reason to believe
that the radical-pair- and magnetic-particle-based magne-
toreceptors contribute to different tasks. Generally, the rad-
ical pair receptor is thought to work purely as a magnetic
compass sense, but without providing map information
(reviewed by Heyers et al. [190]). The lines of evidence that
support this are behavioral studies which show that the
magnetic compass in birds is functional only in light of spe-
cific wavelengths –birds are blind to the magnetic field in
the red and yellow part of the light spectrum [179, 191, 192].
However, it appears that they choose their appropriate
migratory direction under longer wavelengths of the spec-
trum, that is, light of blue or green wavelengths [179, 191,
192]. Another finding supporting radical-pair-based mag-
netic compass orientation is that fast-oscillating weak radio
frequency fields disrupt a bird’s ability to orientate to mag-
netic cues [193–195]. Fast-oscillating weak radio frequency
fields can act as a diagnostic tool to test the involvement of a
radical pair process, because they are too weak (and oscil-
late too fast) to affect a magnetic-particle-based mechanism
but should interfere with the electrons involved in the rad-
ical pair formation process.
Behavioral and electrophysiological evidence in favor of a
magnetite-based magnetoperception mechanism have
been obtained in the olfactory regions in fish [196]. In other
species, magnetic particles have been found in animals
such as the Caribbean spiny lobster [197] and in the heads
of bats [198].
There is also evidence supporting a magnetite receptor
that may be located in a bird’s beak area and functions
as a magnetic map sense (for a review of the magnetic
map in birds, see [190]). This is supported by several behav-
ioral studies that tested performance after lesioning of the
trigeminal nerve. In one experiment‚pigeons were taught
to respond to the presence of magnetic anomalies [199].
When they had anesthesia applied to their upper beaks,
they were unable to detect the magnetic anomaly [199].
More specifically, the magnetite magnetoreceptor seems
to be related to a nerve that runs through the bird beak
called the trigeminal nerve, which may transmit magnetor-
eception information to the nervous system [200, 201]. In
the same experiment mentioned above with pigeons, they
were unable to respond to the magnetic information when
their trigeminal nerve was severed [199]. This was further
corroborated with a similar study on Pekin ducks [202]. The
connection between this magnetite receptor, the trigeminal
nerve, and the navigational map was supported when it was
shown that birds need the trigeminal nerve to correct for a
displacement to an area they have not been to before,
1000 km away from where they were caught [203]. The
presence of magnetic material has been reported in birds
[188, 204], but the magnetite-containing structures were
later be shown to be macrophages and the mineral deposits
did not seem to be connected to nervous tissue, which
would be required for a sensory task [205]. So, as of now,
evidence suggests that in birds the magnetite system in
the beak may be functioning as a map/positional sense used
in navigation and the radical pair mechanism functions as a
compass to identify the poleward direction (for a review,
see [190]).
54.4 Conclusions and Perspectives
The last several decades have seen a great evolution in our
understanding in animal navigation and orientation. What
has been uncovered is that animals have a sophisticated
sensory repertoire that they can use in combination,
enabling them to efficiently complete their movement tasks
across both short and long distances with great versatility.
But as our knowledge in this field expands, we are also
becoming ever more aware of how increasing urbanization
and pollution, in its varying forms, may be interfering with
an animal’s ability to use directional cues from their envi-
ronment. For instance, light cues used for orientation, like
the stars or polarized light, can be masked by nocturnal
artificial light pollution, especially in urban areas [206].
Increasing man-made electromagnetic noise pollution aris-
ing from wireless communication technology was recently
found to interfere with the magnetic compass of birds [195],
and alteration of the chemical environment via air pollu-
tion and aquatic pollution may impact the homing abilities
of animals that rely on olfactory cues [207, 208]. These find-
ings are just a few examples that highlight the importance
of this research and the growing necessity to explore how
our changing world is affecting the orientation and naviga-
tional abilities of the animals we share our space with.
54.4 Conclusions and Perspectives 1701
References
1F. Bairlein et al., “Cross-hemisphere migration of a 25 g
songbird,”Biol. Lett., vol. 8, no. 4, p. 505 LP–507,
August 2012.
2T.W. Horton et al., “Straight as an arrow: Humpback
whales swim constant course tracks during long-distance
migration,”Biol. Lett., vol. 7, no. 5, p. 674 LP–679,
October 2011.
3T.L. Guttridge et al., “Philopatry and regional
connectivity of the Great Hammerhead Shark, Sphyrna
mokarran in the U.S. and Bahamas,”Front. Mar. Sci.,
vol. 4, p. 3, 2017.
4M. Béguer-Pon, M. Castonguay, S. Shan, J. Benchetrit, and
J.J. Dodson, “Direct observations of American eels
migrating across the continental shelf to the Sargasso
Sea,”Nat. Commun., vol. 6, p. 8705, October 2015.
5E. Warrant et al., “The Australian Bogong Moth Agrotis
infusa: A long-distance nocturnal navigator,”Front.
Behav. Neurosci., vol. 10, p. 77, 2016.
6C. Stefanescu, D.X. Soto, G. Talavera, R. Vila, and K.A.
Hobson, “Long-distance autumn migration across the
Sahara by painted lady butterflies: Exploiting resource
pulses in the tropical savannah,”Biol. Lett., vol. 12, no. 10,
October 2016.
7P. Luschi, G.C. Hays, C. Del Seppia, R. Marsh, and F. Papi,
“The navigational feats of green sea turtles migrating from
Ascension Island investigated by satellite telemetry,”Proc.
R. Soc. London. Ser. B Biol. Sci., vol. 265, no. 1412, p. 2279
LP–2284, December 1998.
8H. Dingle, M. Zalucki, W. Rochester, and T. Armijo-
Prewitt, “Distribution of the monarch butterfly, Danaus
plexippus (L.)(Lepidoptera: Nymphalidae), in western
North America,”Biol. J. Linn. Soc., vol. 85, no. 4, pp. 491–
500, 2005.
9K. Rasmussen et al., “Southern Hemisphere humpback
whales wintering off Central America: insights from
water temperature into the longest mammalian
migration,”Biol. Lett., vol. 3, no. 3, pp. 302–305, 2007.
10 J.A. Musick and C. Limpus, “Habitat utilization and
migration in juvenile sea turtles,”Biol. sea turtles, pp. 137–
163, 1997.
11 A.B. Bolten et al., “Transatlantic developmental
migrations of loggerhead sea turtles demonstrated by
mtDNA sequence analysis,”Ecol. Appl., vol. 8, no. 1, pp.
1–7, 1998.
12 M. Lerche-Jørgensen, M. Willemoes, A. P. Tøttrup, K.R.S.
Snell, and K. Thorup, “No apparent gain from continuing
migration for more than 3000 kilometres: Willow
warblers breeding in Denmark winter across the entire
northern Savannah as revealed by geolocators,”Mov.
Ecol., vol. 5, no. 1, 2017.
13 P.F. Battley et al., “Contrasting extreme long-distance
migration patterns in bar-tailed godwits Limosa
lapponica,”J. Avian Biol., vol. 43, no. 1, pp. 21–32, 2012.
14 G. Kramer, “Wird die Sonnehohe bei der
Heimfindeorientierung verwertet?,”J. f ür Ornithol.,
vol. 94, pp. 201–219, 1953.
15 K. Able, “The concepts and terminology of bird
navigation,”J. Avian Biol., vol. 32, no. 2, pp. 174–
183, 2001.
16 C. Merlin, S. Heinze, and S.M. Reppert, “Unraveling
navigational strategies in migratory insects,”Curr. Opin.
Neurobiol., vol. 22, no. 2. pp. 353–361, 2012.
17 R. Muheim, J. Boström, S. Åkesson, and M. Liedvogel,
“Sensory mechanisms of animal orientation and
navigation,”Anim. Mov. Across Scales, pp. 179–194, 2014.
18 A.C. Perdeck, “Two types of orientation in migrating
starlings, Sturnus yulgaris L., and Chaffinches, Fringilla
coelebs L., as revealed by displacement experiments,”
Ardea, vol. 38–90, pp. 1–2, January 2002.
19 M. Liedvogel, S. Åkesson, and S. Bensch, “The genetics of
migration on the move,”Trends Ecol. Evol., vol. 26, no. 11.
pp. 561–569, 2011.
20 T. Mueller, R.B. O’Hara, S.J. Converse, R.P. Urbanek, and
W.F. Fagan, “Social learning of migratory performance,”
Science (80-.)., vol. 341, no. 6149, pp. 999–1002, 2013.
21 C.S. Teitelbaum et al., “Experience drives innovation of
new migration patterns of whooping cranes in response to
global change,”Nat. Commun., vol. 7, 2016.
22 A.P. Nesterova, A. Flack, E.E. van Loon, F. Bonadonna,
and D. Biro, “The effect of experienced individuals on
navigation by king penguin chick pairs,”Anim. Behav.,
vol. 104, pp. 69–78, 2015.
23 A. Berdahl et al., “Collective animal navigation and
migratory culture: From theoretical models to empirical
evidence,”bioRxiv, p. 230219, 2018.
24 D. Biro, D.J.T. Sumpter, J. Meade, and T. Guilford, “From
compromise to leadership in pigeon homing,”Curr. Biol.,
vol. 16, no. 21, pp. 2123–2128, 2006.
25 G. Dell’Ariccia, G. Dell’Omo, D.P. Wolfer, and H.P. Lipp,
“Flock flying improves pigeons’homing: GPS track
analysis of individual flyers versus small groups,”Anim.
Behav., vol. 76, no. 4, pp. 1165–1172, 2008.
26 F. Bonadonna, S. Benhamou, and P. Jouventin,
“Orientation in ‘featureless’environments: The extreme
case of pelagic birds BT,”Avian Migration, 2003, pp.
367–377.
27 B. J. Frost and H. Mouritsen, “The neural mechanisms of
long distance animal navigation,”Curr. Opin. Neurobiol.,
vol. 16, no. 4, pp. 481–488, 2006.
28 H. Mouritsen, D. Heyers, and O. Güntürkün, “The neural
basis of long-distance navigation in birds,”Annu. Rev.
Physiol., vol. 78, no. 1, pp. 133–154, February 2016.
1702 54 Orientation and Navigation in the Animal World
29 G. Kramer, “Über Richtungstendenzen bei der
nächtlichen Zugunruhe gekäfigter Vögel,”Ornithol. als
Biol. Wiss., pp. 269–283, 1949.
30 C. Eikenaar, T. Klinner, K.L. Szostek, and F. Bairlein,
“Migratory restlessness in captive individuals predicts
actual departure in the wild,”Biol. Lett., vol. 10, no. 4, pp.
20140154–20140154, 2014.
31 S.T. Emlen and J. T. Emlen, “A technique for recording
migratory orientation of captive birds,”Source Auk,
vol. 83, no. 3, pp. 361–367, 1966.
32 R.L. Nesbit, J.K. Hill, I.P. Woiwod, D. Sivell, K.J.
Bensusan, and J.W. Chapman, “Seasonally adaptive
migratory headings mediated by a sun compass in the
painted lady butterfly, Vanessa cardui,”Anim. Behav.,
vol. 78, no. 5, pp. 1119–1125, 2009.
33 T. Guilford and G.K. Taylor, “The sun compass revisited,”
Anim. Behav., vol. 97, pp. 135–143, November 2014.
34 J. C. Dunlap, “Molecular bases for circadian clocks,”Cell,
vol. 96, no. 2, pp. 271–290, January 1999.
35 R. Refinetti, Circadian Physiology, 3rd Ed., Boca Raton:
CRC Press, 2016.
36 K. Schmidt-Koenig, J.U. Ganzhorn, and R. Ranvaud, “The
sun compass,”Orientation in Birds (ed. P. Berthold),
Basel: Birkhäuser Basel, 1991, pp. 1–15.
37 Perez, S. M., Taylor, O. R., & Jander, R. (1997). A
sun compass in monarch butterflies. Nature, 387(6628),
29–29.
38 H. Mouritsen, J. Atema, M.J. Kingsford, and G. Gerlach,
“Sun compass orientation helps coral reef fish larvae
return to their natal reef,”PLoS One, vol. 8, no. 6, p.
e66039, June 2013.
39 K. Adler and J.B. Phillips, “Orientation in a desert lizard
(Uma notata): Time-compensated compass movement
and polarotaxis,”J. Comp. Physiol. A, vol. 156, no. 4, pp.
547–552, 1985.
40 C.T. DeRosa and D.H. Taylor, “Sun-compass orientation
in the painted Turtle, Chrysemys picta (Reptilia,
Testudines, Testudinidae),”J. Herpetol., vol. 12, no. 1, pp.
25–28, 1978.
41 S.L. Fluharty, D.H. Taylor, and G.W. Barrett, “Sun-
compass orientation in the Meadow Vole, Microtus
pennsylvanicus,”J. Mammal., vol. 57, no. 1, pp. 1–9,
Feb. 1976.
42 D.H. Taylor and D.E. Ferguson, “Extraoptic celestial
orientation in the southern cricket frog Acris gryllus,”
Science (80-.)., vol. 168, no. 3929, pp. 390–392, 1970.
43 C. Merlin, R.J. Gegear, and S.M. Reppert, “Antennal
circadian clocks coordinate sun compass orientation in
migratory monarch butterflies,”Science, vol. 325, no.
5948, pp. 1700–1704, September 2009.
44 H. Mouritsen and B.J. Frost, “Virtual migration in
tethered flying monarch butterflies reveals their
orientation mechanisms,”Proc. Natl. Acad. Sci. U. S. A.,
vol. 99, no. 15, pp. 10162–10166, July 2002.
45 O. Froy, A.L. Gotter, A.L. Casselman, and S.M. Reppert,
“Illuminating the circadian clock in monarch butterfly
migration,”Science (80-.)., vol. 300, no. 5623, p. 1303 LP–
1305, May 2003.
46 S.M. Reppert, R.J. Gegear, and C. Merlin, “Navigational
mechanisms of migrating monarch butterflies,”Trend.
Neurosci., vol. 33, no. 9. pp. 399–406, 2010.
47 P.A. Guerra, R.J. Gegear, and S.M. Reppert, “A magnetic
compass aids monarch butterfly migration,”Nat.
Commun., vol. 5, p. 4164, June 2014.
48 P.A. Guerra, C. Merlin, R.J. Gegear, and S.M. Reppert,
“Discordant timing between antennae disrupts sun
compass orientation in migratory monarch butterflies,”
Nat. Commun., vol. 3, p. 958, July 2012.
49 G. Kramer, “Eine neue Methode zur Erforschung der
Zugorientierung und die bisher damit erzielten
Ergebnisse,”in Proc. Int. Ornithol. Congr, 1951, vol. 10, pp.
269–280.
50 K. Schmidt-Koenig, “Experimentelle Einflußnahme auf
die 24-Stunden-Periodik bei Brieftauben und deren
Auswirkungen unter besonderer Berücksichtigung des
Heimfindevermögens,”Ethology, vol. 15, no. 3, pp. 301–
331, 1958.
51 W. Wiltschko, R. Wiltschko, and W.T. Keeton, “Effects of
a‘permanent’clock-shift on the orientation of young
homing pigeons,”Behav. Ecol. Sociobiol., vol. 1, no. 3, pp.
229–243, 1976.
52 W. Wiltschko, R. Wiltschko, and W.T. Keeton, “The effect
of a ‘permanent’clock-shift on the orientation of
experienced homing pigeons –I. Experiments in Ithaca,
New York, USA,”Behav. Ecol. Sociobiol., vol. 15, no. 4, pp.
263–272, 1984.
53 U. Munro and R. Wiltschko, “Clock-shift experiments
with migratory yellow-faced honeyeaters,
Lichenostomus chrysops (Meliphagidae), an
Australian day migrating bird,”J. Exp. Biol., vol. 181,
pp. 233–244, 1993.
54 S. Åkesson, N. Jonzén, J. Pettersson, M. Rundberg, and R.
Sandberg, “Effects of magnetic manipulations on
orientation: Comparing diurnal and nocturnal passerine
migrants on Capri, Italy in autumn,”Ornis Svecica,
vol. 16, pp. 55–61, 2006.
55 W. Wiltschko and R. Wiltschko, “Homing pigeons as a
model for avian navigation?,”J. Avian Biol., vol. 48, no. 1,
pp. 66–74, 2017.
56 N. Chernetsov, “Compass systems,”J. Comp. Physiol. A,
vol. 203, no. 6–7, pp. 447–453, 2017.
57 O. Padget et al., “In situ clock shift reveals that the sun
compass contributes to orientation in a Pelagic Seabird,”
Curr. Biol., vol. 28, no. 2, p. 275–279.e2, January 2018.
References 1703
58 G. Horváth, Polarized light and Polarization Vision in
Animal Sciences, 2014.
59 K.V. Frisch, “Die Polarisation des Himmelslichtes als
orientierender Faktor bei den Tänzen der Bienen,”
Experientia, vol. 5, no. 4, pp. 142–148, 1949.
60 M. Dacke and M.V. Srinivasan, “Two odometers in
honeybees?,”J. Exp. Biol., vol. 211, no. 20, pp. 3281–
3286, 2008.
61 P. Kraft, C. Evangelista, M. Dacke, T. Labhart, and M.V.
Srinivasan, “Honeybee navigation: Following routes
using polarized-light cues,”Philos. Trans. R. Soc. B Biol.
Sci., vol. 366, no. 1565, pp. 703–708, 2011.
62 K. Von Frisch, Die Tänze der Bienen, vol. 1, 1946.
63 C. Evangelista, P. Kraft, M. Dacke, T. Labhart, and M.V.
Srinivasan, “Honeybee navigation: Critically examining
the role of the polarization compass,”Philos. Trans. R. Soc.
B Biol. Sci., vol. 369, no. 1636, 2014.
64 M. Müller and R. Wehner, “Path integration in desert
ants, Cataglyphis fortis,”Proc. Natl. Acad. Sci., vol. 85, no.
14, pp. 5287–5290, 1988.
65 R. Wehner and M. Müller, “The significance of direct
sunlight and polarized skylight in the ant’s celestial
system of navigation,”Proc. Natl. Acad. Sci., vol. 103, no.
33, pp. 12575–12579, 2006.
66 F. Lebhardt, J. Koch, and B. Ronacher, “The polarization
compass dominates over idiothetic cues in path
integration of desert ants,”J. Exp. Biol., vol. 215, no. 3, pp.
526–535, 2012.
67 W.J. Gehring and R. Wehner, “Heat shock protein
synthesis and thermotolerance in Cataglyphis, an ant
from the Sahara desert.,”Proc. Natl. Acad. Sci., vol. 92, no.
7, pp. 2994–2998, 1995.
68 M. Wittlinger, R. Wehner, and H. Wolf, “The desert ant
odometer: a stride integrator that accounts for stride
length and walking speed,”J. Exp. Biol., vol. 210, no. 2, pp.
198–207, 2007.
69 M. Wittlinger, R. Wehner, and H. Wolf, “The ant
odometer: Stepping on stilts and stumps,”Science (80-.).,
vol. 312, no. 5782, pp. 1965–1967, 2006.
70 S.F. Reid, A. Narendra, J.M. Hemmi, and J. Zeil,
“Polarised skylight and the landmark panorama provide
night-active bull ants with compass information during
route following,”J. Exp. Biol., vol. 214, no. 3, pp. 363–
370, 2011.
71 C.A. Freas, A. Narendra, C. Lemesle, and K. Cheng,
“Polarized light use in the nocturnal bull ant,
Myrmecia midas.,”R. Soc. open Sci., vol. 4, no. 8,
p. 170598, 2017.
72 M. Dacke, P. Nordström, and C.H. Scholtz, “Twilight
orientation to polarised light in the crepuscular dung
beetle Scarabaeus zambesianus,”J. Exp. Biol., vol. 206, no.
9, pp. 1535–1543, 2003.
73 B. el Jundi et al., “Neural coding underlying the cue
preference for celestial orientation,”Proc. Natl. Acad.
Sci., 2015.
74 M. Dacke, D.-E. Nilsson, C.H. Scholtz, M. Byrne, and E.J.
Warrant, “Animal behaviour: Insect orientation to
polarized moonlight,”Nature, vol. 424, no. 6944,
pp. 33–33, 2003.
75 T. Labhart and E.P. Meyer, “Detectors for polarized
skylight in insects: A survey of ommatidial
specializations in the dorsal rim area of the
compound eye,”Microsc. Res. Tech., vol. 47, no. 6, pp. 368–
379, 1999.
76 E. Warrant and D.-E. Nilsson, Invertebrate Vision.
Cambridge University Press, 2006.
77 D.E. Nilsson, T. Labhart, and E. Meyer, “Photoreceptor
design and optical properties affecting polarization
sensitivity in ants and crickets,”J. Comp. Physiol. A,
vol. 161, no. 5, pp. 645–658, 1987.
78 G. Horváth et al., “Celestial polarization patterns
sufficient for Viking navigation with the naked eye:
detectability of Haidinger’s brushes on the sky versus
meteorological conditions,”R. Soc. Open Sci., vol. 4, no. 2,
February 2017.
79 J.B. Phillips and F.R. Moore, “Calibration of the sun
compass by sunset polarized light patterns in a migratory
bird,”Behav. Ecol. Sociobiol., vol. 31, no. 3, pp. 189–
193, 1992.
80 W.W. Cochran, H. Mouritsen, and M. Wikelski,
“Migrating songbirds recalibrate their magnetic compass
daily from twilight cues,”Science (80-.)., vol. 304, no. 5669,
pp. 405–408, 2004.
81 R. Muheim, J.B. Phillips, and S. Åkesson, “Polarized light
cues underlie compass calibration in migratory
songbirds,”Science (80-.)., vol. 313, no. 5788, pp. 837–
839, 2006.
82 R. Muheim, J.B. Phillips, and M.E. Deutschlander,
“White-throated sparrows calibrate their magnetic
compass by polarized light cues during both autumn
and spring migration,”J. Exp. Biol., vol. 212, no. 21,
pp. 3466–3472, 2009.
83 R. Muheim, “Behavioural and physiological mechanisms
of polarized light sensitivity in birds.,”Philos. Trans. R.
Soc. Lond. B. Biol. Sci., vol. 366, no. 1565, pp. 763–
771, 2011.
84 R.A. Holland, I. Borissov, and B.M. Siemers, “A nocturnal
mammal, the greater mouse-eared bat, calibrates a
magnetic compass by the sun,”Proc. Natl. Acad. Sci.,
vol. 107, no. 15, pp. 6941–6945, 2010.
85 S. Greif, I. Borissov, Y. Yovel, and R.A. Holland, “A
functional role of the skys polarization pattern for
orientation in the greater mouse-eared bat,”Nat.
Commun., vol. 5, 2014.
1704 54 Orientation and Navigation in the Animal World
86 J. McGregor, S. Temple, and G. Horváth, “Human
polarization sensitivity,”Polarized Light and Polarization
Vision in Animal Sciences (ed. G. Horváth), Berlin,
Heidelberg: Springer Berlin Heidelberg, 2014, pp.
303–315.
87 P. Kerlinger and F.R. Moore, “Atmospheric structure and
avian migration,”in Current Ornithology, no. January
1989, pp. 109–142.
88 T. Alerstam, “Flight by night or day? Optimal daily timing
of bird migration,”J. Theor. Biol., vol. 258, no. 4, pp. 530–
536, 2009.
89 F. Sauer, “Die Sternenorientierung nächtlich ziehender
Grasmücken (Sylvia atricapilla, borin und curruca),”
Zeitschrift Tierpsychol., vol. 14, no. 1, pp. 29–70, 1957.
90 S.T. Emlen, “Migratory orientation in the Indigo Bunting,
Passerina cyanea: Part I: Evidence for use of celestial
cues,”Auk, vol. 84, no. 3, pp. 309–342, 1967.
91 S.T. Emlen, “Celestial rotation: its importance in the
development of migratory orientation,”Science (80-.).,
vol. 170, no. 3963, pp. 1198–201, 1970.
92 S.T. Emlen, “Migratory orientation in the Indigo Bunting,
Passerina cyanea. Part II: Mechanism of celestial
orientation,”Auk, vol. 84, no. 4, pp. 463–489, 1967.
93 A. Michalik, B. Alert, S. Engels, N. Lefeldt, and H.
Mouritsen, “Star compass learning: How long does it
take?,”J. Ornithol., vol. 155, no. 1, pp. 225–234, 2014.
94 W. Wiltschko, P. Daum, A. Fergenbauer-Kimmel, and R.
Wiltschko, “The development of the star compass in
Garden Warblers, Sylvia borin,”Ethology, vol. 74, no. 4,
pp. 285–292, 1987.
95 M. Dacke, E. Baird, M. Byrne, C.H. Scholtz, and E.J.
Warrant, “Dung beetles use the milky way for
orientation,”Curr. Biol., vol. 23, no. 4, pp. 298–300,
February 2013.
96 B. Mauck, D. Brown, W. Schlosser, F. Schaeffel, and G.
Dehnhardt, “How a harbor seal sees the night sky,”
Marine Mammal Sci., vol. 21, no. 4, 646–656, 2005.
97 B. Mauck, N. Gläser, W. Schlosser, and G. Dehnhardt,
“Harbour seals (Phoca vitulina) can steer by the stars,”
Anim. Cogn., vol. 11, no. 4, pp. 715–718, 2008.
98 B. Alert, A. Michalik, S. Helduser, H. Mouritsen, and O.
Güntürkün, “Perceptual strategies of pigeons to detect a
rotational centre –A hint for star compass learning?,”
PLoS One, vol. 10, no. 3, 2015.
99 R.M. Douglas, A. Neve, J.P. Quittenbaum, N.M. Alam,
and G.T. Prusky, “Perception of visual motion coherence
by rats and mice,”Vision Res., vol. 46, no. 18, pp. 2842–
2847, 2006.
100 K.L. Woo, G. Rieucau, and D. Burke, “Computer-
animated stimuli to measure motion sensitivity:
Constraints on signal design in the Jacky dragon,”Curr.
Zool., vol. 63, no. 1, pp. 75–84, 2017.
101 W.F. Bischof, S.L. Reid, D.R.W. Wylie, and M.L. Spetch,
“Perception of coherent motion in random dot displays by
pigeons and humans,”Percept. Psychophys., vol. 61, no. 6,
pp. 1089–1101, 1999.
102 J.J. Foster, J. Smolka, D.-E. Nilsson, and M. Dacke, “How
animals follow the stars,”Proc. R. Soc. B Biol. Sci., vol. 285,
no. 1871, p. 20172322, 2018.
103 B.W. Ache and J.M. Young, “Olfaction: Diverse species,
conserved principles,”Neuron, vol. 48, no. 3, pp. 417–430,
November 2005.
104 L. Sela and N. Sobel, “Human olfaction: A constant state
of change-blindness,”Exp. Brain Res., vol. 205, no. 1. pp.
13–29, 2010.
105 J.P. Croxall, Seabirds. Feeding ecology and role in marine
ecosystems. 1987.
106 B.G. Bang, “The olfactory apparatus of tubenosed birds
(Procellariiformes),”Cells Tissues Organs, vol. 65, no. 1–3,
pp. 391–415, 1966.
107 G.A. Nevitt, “Sensory ecology on the high seas: The odor
world of the procellariiform seabirds,”J. Exp. Biol.,
vol. 211, no. 11, pp. 1706–1713, 2008.
108 B.G. Bang and S. Cobb, “The size of the olfactory bulb in
108 species of birds,”Auk, vol. 85, no. 1, pp. 55–61, 1968.
109 G.A. Nevitt, R.R. Veit, and P. Kareiva, “Dimethyl sulphide
as a foraging cue for Antarctic Procellariiform seabirds,”
Nature, vol. 376, no. 6542, pp. 680–682, 1995.
110 G. Dell’Ariccia, A. Celerier, M. Gabirot, P. Palmas, B.
Massa, and F. Bonadonna, “Olfactory foraging in
temperate waters: Sensitivity to dimethylsulphide of
shearwaters in the Atlantic Ocean and Mediterranean
Sea,”J. Exp. Biol., vol. 217, no. 10, pp. 1701–1709, 2014.
111 J.W.H. Dacey and S.G. Wakeham, “Oceanic
dimethylsulfide: Production during zooplankton grazing
on phytoplankton,”Science (80-.)., vol. 233, no. 4770, pp.
1314–1316, 1986.
112 G.A. Nevitt, “The neuroecology of dimethyl sulfide:
A global-climate regulator turned marine infochemical,”
Integr. Comp. Biol., vol. 51, no. 5, pp. 819–825, 2011.
113 S. Kowalewsky, M. Dambach, B. Mauck, and G.
Dehnhardt, “High olfactory sensitivity for dimethyl
sulphide in harbour seals,”Biol. Lett., vol. 2, no. 1, pp. 106–
109, 2006.
114 G.B. Cunningham, V. Strauss, and P.G. Ryan, “African
penguins (Spheniscus demersus) can detect dimethyl
sulphide, a prey-related odour,”J. Exp. Biol., vol. 211, no.
19, pp. 3123–3127, 2008.
115 L. Amo, M.Á. Rodríguez-Gironés, and A. Barbosa,
“Olfactory detection of dimethyl sulphide in a krill-eating
Antarctic penguin,”Marine Ecology Progress Series,
vol. 474. pp. 277–285, 2013.
116 C.S. Endres and K.J. Lohmann, “Perception of dimethyl
sulfide (DMS) by loggerhead sea turtles: a possible
References 1705
mechanism for locating high-productivity oceanic regions
for foraging,”J. Exp. Biol., vol. 215, no. 20, pp. 3535–
3538, 2012.
117 A.D.M. Dove, “Foraging and ingestive behaviors of whale
sharks, Rhincodon typus, in response to chemical
stimulus cues,”Biol. Bull., vol. 228, no. 1, pp. 65–74, 2015.
118 J.L. DeBose, S.C. Lema, and G.A. Nevitt,
“Dimethylsulfoniopropionate as a foraging cue for reef
fishes,”Science, vol. 319, no. 5868. p. 1356, 2008.
119 J.C. Montgomery, A. Jeffs, S.D. Simpson, M. Meekan, and
C. Tindle, “Sound as an orientation cue for the pelagic
larvae of reef fishes and decapod crustaceans,”Advances
in Marine Biology, vol. 51. pp. 143–196, 2006.
120 M.A. Foretich, C.B. Paris, M. Grosell, J.D. Stieglitz, and D.
D. Benetti, “Dimethyl sulfide is a chemical attractant for
reef fish larvae,”Sci. Rep., vol. 7, no. 1, 2017.
121 A. Gagliardo, “Forty years of olfactory navigation in
birds,”J. Exp. Biol., vol. 216, no. 12, pp. 2165–2171, 2013.
122 A. Gagliardo, “Having the nerve to home: trigeminal
magnetoreceptor versus olfactory mediation of homing in
pigeons,”J. Exp. Biol., vol. 209, no. 15, pp. 2888–
2892, 2006.
122 F. Papi, L. Fiore, V. Fiaschi, and S. Benvenuti, “The
influence of olfactory nerve section on the homing
capacity of carrier pigeons,”Monit. Zool. Ital. –Ital. J.
Zool., vol. 5, no. 4, pp. 265–267, 1971.
124 H.G. Wallraff, “Weitere Volierenversuche mit
Brieftauben: Wahrscheinlicher Einfluß dynamischer
Faktorens der Atmosphäre auf die Orientierung,”Z. Vgl.
Physiol., vol. 68, no. 2, pp. 182–201, 1970.
125 P. Ioalé, F. Papi, V. Fiaschi, and N. E. Baldaccini, “Pigeon
navigation: Effects upon homing behaviour by reversing
wind direction at the loft,”J. Comp. Physiol. □A, vol. 128,
no. 4, pp. 285–295, 1978.
126 P. Ioalè, “Further investigations on the homing behaviour
of pigeons subjected to reverse wind direction at the loft,”
Monit. Zool. Ital. - Ital. J. Zool., vol. 14, no. 1–2, pp. 77–
87, 1980.
127 F. Papi, P. Ioalé, V. Fiaschi, S. Benvenuti, and N.E.
Baldaccini, “Olfactory navigation of pigeons: The effect of
treatment with odorous air currents,”J. Comp. Physiol. A,
vol. 94, no. 3, pp. 187–193, 1974.
128 G.A. Nevitt and F. Bonadonna, “Sensitivity to dimethyl
sulphide suggests a mechanism for olfactory navigation
by seabirds,”Biol. Lett., vol. 1, no. 3, pp. 303–305, 2005.
129 B. Massa, S. Benvenuti, P. Ioalè, M. Lo Valvo, and F. Papi,
“Homing of Cory’s shearwaters (Calonectris diomedea)
carrying magnets,”Bolletino di Zool., vol. 58, no. 3, pp.
245–247, 1991.
130 A. Gagliardo, J. Bried, P. Lambardi, P. Luschi, M.
Wikelski, and F. Bonadonna, “Oceanic navigation in
Cory’s shearwaters: Evidence for a crucial role of olfactory
cues for homing after displacement,”J. Exp. Biol., vol. 216,
no. 15, pp. 2798–2805, 2013.
131 E. Pollonara, P. Luschi, T. Guilford, M. Wikelski, F.
Bonadonna, and A. Gagliardo, “Olfaction and
topography, but not magnetic cues, control navigation in
a pelagic seabird: Displacements with shearwaters in the
Mediterranean Sea,”Sci. Rep., vol. 5, 2015.
132 A.P. Nosal, Y. Chao, J.D. Farrara, F. Chai, and P.A.
Hastings, “Olfaction contributes to pelagic navigation in a
coastal shark,”PLoS One, vol. 11, no. 1, 2016.
133 J.M. Gardiner, N.M. Whitney, and R.E. Hueter, “Smells
like home: The role of olfactory cues in the homing
behavior of blacktip sharks, carcharhinus limbatus,”in
Integrative and Comparative Biology, 2015, vol. 55, no. 3,
pp. 495–506.
134 M.C. Healey, Life history of Chinook Salmon
(Oncorhynchus tshawytscha). 1991.
135 T.P. Quinn, “Behavior and ecology of Pacific Salmon and
Trout,”Fish Fish., vol. 7, pp. 75–76, 2004.
136 N.F. Putman et al., “An inherited magnetic map guides
ocean navigation in juvenile pacific salmon,”Curr. Biol.,
vol. 24, no. 4, pp. 446–450, 2014.
137 N.N. Bett and S.G. Hinch, “Olfactory navigation during
spawning migrations: A review and introduction of the
Hierarchical Navigation Hypothesis.,”Biol. Rev. Camb.
Philos. Soc., vol. 91, no. 3, pp. 728–59, August 2016.
138 M. Wikelski et al., “True navigation in migrating gulls
requires intact olfactory nerves,”Sci. Rep., vol. 5, 2015.
139 R.A. Holland et al., “Testing the role of sensory systems in
the migratory heading of a songbird,”J. Exp. Biol.,
vol. 212, no. 24, pp. 4065–4071, 2009.
140 J.A. Tarduno, E.G. Blackman, and E.E. Mamajek,
“Detecting the oldest geodynamo and attendant shielding
from the solar wind: Implications for habitability,”Phys.
Earth Planet. Inter., vol. 233. pp. 68–87, 2014.
141 J.A. Tarduno, R.D. Cottrell, W.J. Davis, F. Nimmo, and R.
K. Bono, “A Hadean to Paleoarchean geodynamo
recorded by single zircon crystals,”Science (80-.)., vol. 349,
no. 6247, pp. 521–524, 2015.
142 D. Wacey, M.R. Kilburn, M. Saunders, J. Cliff, and M.D.
Brasier, “Microfossils of sulphur-metabolizing cells in 3.4-
billion-year-old rocks of Western Australia,”Nat. Geosci.,
vol. 4, no. 10, pp. 698–702, 2011.
143 A.P. Nutman, V.C. Bennett, C.R.L. Friend, M.J. Van
Kranendonk, and A.R. Chivas, “Rapid emergence of life
shown by discovery of 3,700-million-year-old microbial
structures,”Nature, vol. 537, no. 7621, pp. 535–538, 2016.
144 F.W. Merkel and W. Wiltschko, “Magnetismus und
richtungsfinden zugunruhiger rotkehlchen (Erithacus
rubecula),”Vogelwarte, vol. 23, no. 1, pp. 71–77, 1965.
145 W. Wiltschko and R. Wiltschko, “Magnetic orientation in
birds,”J. Exp. Biol., vol. 199, no. Pt. 1, pp. 29–38, 1996.
1706 54 Orientation and Navigation in the Animal World
146 W. Wiltschko and R. Wiltschko, “Magnetic compass of
European Robins,”Science (80-.)., vol. 176, no. 4030, pp.
62–64, 1972.
147 W. Wiltschko, “Über den Einfluß statischer Magnetfelder
auf die Zugorientierung der Rotkehlchen (Erithacus
rubecula),”Zeitschrift f??r Tierpsychologie, vol. 25, no. 5,
pp. 537–558, 1968.
148 W. Wiltschko, “Further analysis of the magnetic compass
of migratory birds,”in Animal Migration, Navigation, and
Homing, 1978, pp. 302–310.
149 W. Wiltschko, K. Stapput, P. Thalau, and R. Wiltschko,
“Avian magnetic compass: Fast adjustment to intensities
outside the normal functional window,”
Naturwissenschaften, vol. 93, no. 6, pp. 300–304, 2006.
150 R. Wiltschko and W. Wiltschko, Magnetic Orientation in
Animals, vol. 33. 1995.
151 R. Freire, U.H. Munro, L.J. Rogers, R. Wiltschko, and W.
Wiltschko, “Chickens orient using a magnetic compass,”
Curr. Biol., vol. 15, no. 16. 2005.
152 N. Keary et al., “Oscillating magnetic field disrupts
magnetic orientation in Zebra finches, Taeniopygia
guttata,”Front. Zool., vol. 6, no. 1, 2009.
153 R. Muheim, N.M. Edgar, K.A. Sloan, and J.B. Phillips,
“Magnetic compass orientation in C57BL/6J mice,”
Learn. Behav. a Psychon. Soc. Publ., vol. 34, no. 4, pp. 366–
373, 2006.
154 R.R. Baker, “Human navigation and magnetoreception:
The Manchester experiments do replicate,”Anim. Behav.,
vol. 35, no. 3, pp. 691–704, 1987.
155 P. Light, M. Salmon, and K.J. Lohmann, “Geomagnetic
orientation of Loggerhead Sea Turtles: Evidence for an
inclination compass,”J. Exp. Biol., vol. 182, no. 1, pp. 1–
10, 1993.
156 S. Marhold, W. Wiltschko, and H. Burda, “A magnetic
polarity compass for direction finding in a subterranean
mammal,”Naturwissenschaften, vol. 84, no. 9, pp. 421–
423, 1997.
157 Y. Wang, Y. Pan, S. Parsons, M. Walker, and S. Zhang,
“Bats respond to polarity of a magnetic field,”Proc. R. Soc.
B Biol. Sci., vol. 274, no. 1627, p. 2901 LP–2905,
November 2007.
158 R.A. Holland, J.L. Kirschvink, T.G. Doak, and M.
Wikelski, “Bats use magnetite to detect the earth’s
magnetic field,”PLoS One, vol. 3, no. 2, 2008.
159 K. Lohmann et al., “Magnetic orientation of spiny lobsters
in the ocean: experiments with undersea coil systems,”J.
Exp. Biol., vol. 198, no. Pt 10, pp. 2041–2048, 1995.
160 H. Mouritsen and T. Ritz, “Magnetoreception and its use
in bird navigation,”Curr. Opin. Neurobiol., vol. 15, no. 4.
pp. 406–414, 2005.
161 T. Fransson, S. Jakobsson, P. Johansson, C. Kullberg, J.
Lind, and A. Vallin, “Bird migration: Magnetic cues
trigger extensive refuelling,”Nature, vol. 414, no. 6859,
pp. 35–36, 2001.
162 K.J. Lohmann, S.D. Cain, S.A. Dodge, and C.M.F.
Lohmann, “Regional magnetic fields as navigational
markers for sea turtles,”Science (80-.)., vol. 294, no. 5541,
pp. 364–366, 2001.
163 M.M. Walker, T.E. Dennis, and J.L. Kirschvink, “The
magnetic sense and its use in long-distance navigation by
animals,”Curr. Opin. Neurobiol., vol. 12, no. 6. pp. 735–
744, 2002.
164 L.C. Boles and K.J. Lohmann, “True navigation and
magnetic maps in spiny lobsters,”Nature, vol. 421, no.
6918, pp. 60–63, 2003.
165 D. Kishkinev, N. Chernetsov, A. Pakhomov, D. Heyers,
and H. Mouritsen, “Eurasian reed warblers compensate
for virtual magnetic displacement,”Curr. Biol., vol. 25, no.
19, pp. R822–R824, 2015.
166 N. Chernetsov, A. Pakhomov, D. Kobylkov, D. Kishkinev,
R.A. Holland, and H. Mouritsen, “Migratory Eurasian
reed warblers can use magnetic declination to solve the
longitude problem,”Curr. Biol., vol. 27, no. 17, p. 2647–
2651.e2, 2017.
167 K.J. Lohmann, C.M.F. Lohmann, L.M. Ehrhart, D.A.
Bagley, and T. Swing, “Geomagnetic map used in sea-
turtle navigation,”Nature, vol. 428, no. 6986, pp. 909–
910, 2004.
168 F. Papi, H.C. Liew, P. Luschi, and E.H. Chan, “Long-range
migratory travel of a green turtle tracked by satellite:
Evidence for navigational ability in the open sea,”Mar.
Biol., vol. 122, no. 2, pp. 171–175, 1995.
169 A.C. Broderick, M.S. Coyne, W.J. Fuller, F. Glen, and B.J.
Godley, “Fidelity and over-wintering of sea turtles,”
Proc. R. Soc. B Biol. Sci., vol. 274, no. 1617, pp. 1533–
1539, 2007.
170 K.J. Lohmann, N.F. Putman, and C.M.F. Lohmann, “The
magnetic map of hatchling loggerhead sea turtles,”Curr.
Opin. Neurobiol., vol. 22, no. 2. pp. 336–342, 2012.
171 N.F. Putman, P. Verley, C.S. Endres, and K.J. Lohmann,
“Magnetic navigation behavior and the oceanic ecology of
young loggerhead sea turtles,”J. Exp. Biol., vol. 218, no. 7,
pp. 1044–1050, 2015.
172 L.C. Naisbett-Jones, N.F. Putman, J.F. Stephenson, S.
Ladak, and K.A. Young, “A magnetic map leads juvenile
European Eels to the Gulf Stream,”Curr. Biol., vol. 27, no.
8, pp. 1236–1240, 2017.
173 J.H. Fischer, M.J. Freake, S.C. Borland, and J.B. Phillips,
“Evidence for the use of magnetic map information by an
amphibian,”Anim. Behav., vol. 62, no. 1, pp. 1–10, 2001.
174 J.B. Phillips, M.J. Freake, J.H. Fischer, and S.C. Borland,
“Behavioral titration of a magnetic map coordinate,”J.
Comp. Physiol. A Neuroethol. Sensory, Neural, Behav.
Physiol., vol. 188, no. 2, pp. 157–160, 2002.
References 1707
175 K. Schulten, C.E. Swenberg, and A. Weiler, “A
biomagnetic sensory mechanism based on magnetic field
modulated coherent electron spin motion,”Zeitschrift
Phys. Chem., vol. 111, no. 1, pp. 1–5, 1978.
176 T. Ritz, S. Adem, and K. Schulten, “A model for
photoreceptor-based magnetoreception in birds,”
Biophys. J., vol. 78, no. 2, pp. 707–718, 2000.
177 J.B. Phillips and S.C. Borland, “Behavioural evidence for
use of a light-dependent magnetoreception mechanism by
a vertebrate,”Nature, vol. 359, no. 6391, pp. 142–
144, 1992.
178 J.B. Phillips and O. Sayeed, “Wavelength-dependent
effects of light on magnetic compass orientation in
Drosophila melanogaster,”J. Comp. Physiol. A, vol. 172,
no. 3, pp. 303–308, 1993.
179 W. Wiltschko, U. Munro, H. Ford, and R. Wiltschko, “Red
light disrupts magnetic orientation of migratory birds,”
Nature, vol. 364, no. 6437, pp. 525–527, 1993.
180 M. E. Deutschlander, S. C. Borland, and J. B. Phillips,
“Extraocular magnetic compass in newts [6],”Nature,
vol. 400, no. 6742. pp. 324–325, 1999.
181 M. Vácha, T. Půžová, and D. Drštková, “Effect of light
wavelength spectrum on magnetic compass orientation in
Tenebrio molitor,”J. Comp. Physiol. A Neuroethol.
Sensory, Neural, Behav. Physiol., vol. 194, no. 10, pp. 853–
859, 2008.
182 J.B. Phillips, P.E. Jorge, and R. Muheim, “Light-
dependent magnetic compass orientation in amphibians
and insects: candidate receptors and candidate molecular
mechanisms,”J. R. Soc. Interface, vol. 7, no. Suppl._2, pp.
S241–S256, 2010.
183 I. Chaves et al., “The cryptochromes: Blue light
photoreceptors in plants and animals,”Annu. Rev. Plant
Biol., vol. 62, no. 1, pp. 335–364, 2011.
184 P.J. Hore and H. Mouritsen, “The radical-pair mechanism
of magnetoreception,”Annu. Rev. Biophys., vol. 45, no. 1,
pp. 299–344, 2016.
185 J.L. Kirschvink and J.L. Gould, “Biogenic magnetite as a
basis for magnetic field detection in animals,”BioSystems,
vol. 13, no. 3, pp. 181–201, 1981.
186 J.L. Kirschvink, M.M. Walker, and C.E. Diebel,
“Magnetite-based magnetoreception,”Curr. Opin.
Neurobiol., vol. 11, no. 4. pp. 462–467, 2001.
187 R.C. Beason and P. Semm, “Magnetic responses of the
trigeminal nerve system of the bobolink (Dolichonyx
oryzivorus),”Neurosci. Lett., vol. 80, no. 2, pp. 229–
234, 1987.
188 G. Fleissner et al., “Ultrastructural analysis of a
putative magnetoreceptor in the beak of homing
pigeons,”J. Comp. Neurol., vol. 458, no. 4, pp. 350–
360, 2003.
189 H. Cadiou and P.A. McNaughton, “Avian magnetite-
based magnetoreception: A physiologist’s perspective,”J.
R. Soc. Interface, vol. 7, no. Suppl._2, pp. S193–S205, 2010.
190 D. Heyers, D. Elbers, M. Bulte, F. Bairlein, and H.
Mouritsen, “The magnetic map sense and its use in fine-
tuning the migration programme of birds,”J. Comp.
Physiol. A: Neuroethol. Sens. Neural. Behav. Physiol.,
vol. 203, no. 6–7. pp. 491–497, 2017.
191 W. Wiltschko and R. Wiltschko, “The effect of yellow and
blue light on magnetic compass orientation in European
robins, Erithacus rubecula,”J. Comp. Physiol. –A Sensory,
Neural, Behav. Physiol., vol. 184, no. 3, pp. 295–299, 1999.
192 R. Muheim and M. Liedvogel, “The light-dependent
magnetic compass,”in Photobiology: The Science of Light
and Life, Third Edition, 2015, pp. 323–334.
193 T. Ritz, P. Thalau, J. B. Phillips, R. Wiltschko, and W.
Wiltschko, “Resonance effects indicate a radical-pair
mechanism for avian magnetic compass,”Nature,
vol. 429, no. 6988, pp. 177–180, 2004.
194 P. Thalau, T. Ritz, K. Stapput, R. Wiltschko, and W.
Wiltschko, “Magnetic compass orientation of migratory
birds in the presence of a 1.315 MHz oscillating field,”
Naturwissenschaften, vol. 92, no. 2, pp. 86–90, 2005.
195 S. Engels et al., “Anthropogenic electromagnetic noise
disrupts magnetic compass orientation in a migratory
bird,”Nature, vol. 509, no. 7500, pp. 353–356, 2014.
196 M.M. Walker, C.E. Diebel, C.V. Haugh, P.M. Pankhurst, J.
C. Montgomery, and C.R. Green, “Structure and function
of the vertebrate magnetic sense,”Nature, vol. 390, no.
6658, pp. 371–376, 1997.
197 K.J. Lohmann, “Magnetic remanence in the Western
Atlantic spiny lobster, Panulirus argus,”J. Exp. Biol.,
vol. 113, pp. 29–41, 1984.
198 L. Tian, W. Lin, S. Zhang, and Y. Pan, “Bat head contains
soft magnetic particles: Evidence from magnetism,”
Bioelectromagnetics, vol. 31, no. 7, pp. 499–503, 2010.
199 C.V. Mora, M. Davison, J. Martin Wild, and M.M. Walker,
“Magnetoreception and its trigeminal mediation in the
homing pigeon,”Nature, vol. 432, no. 7016, pp. 508–
511, 2004.
200 M.N. Williams and J.M. Wild, “Trigeminally innervated
iron-containing structures in the beak of homing pigeons,
and other birds,”Brain Res., vol. 889, no. 1–2, pp. 243–
246, 2001.
201 D. Heyers, M. Zapka, M. Hoffmeister, J.M. Wild, and H.
Mouritsen, “Magnetic field changes activate the
trigeminal brainstem complex in a migratory bird,”Proc.
Natl. Acad. Sci., vol. 107, no. 20, pp. 9394–9399, 2010.
202 R. Freire, E. Dunston, E.M. Fowler, G.L. McKenzie, C.T.
Quinn, and J. Michelsen, “Conditioned response to a
magnetic anomaly in the Pekin duck (Anas platyrhynchos
1708 54 Orientation and Navigation in the Animal World
domestica) involves the trigeminal nerve,”J. Exp. Biol.,
vol. 215, no. 14, pp. 2399–2404, 2012.
203 D. Kishkinev, N. Chernetsov, D. Heyers, and H.
Mouritsen, “Migratory reed warblers need intact
trigeminal nerves to correct for a 1,000 km eastward
displacement,”PLoS One, vol. 8, no. 6, 2013.
204 G. Falkenberg, G. Fleissner, K. Schuchardt, M.
Kuehbacher, P. Thalau, H. Mouritsen, D. Heyers, G.
Wellenreuther, and G. Fleissner, “Avian
magnetoreception: elaborate iron mineral containing
dendrites in the upper beak seem to be a common feature
of birds,”PLoS One, vol. 5, no. 2, p. e9231, 2010.
205 C.D. Treiber, M.C. Salzer, J. Riegler, N. Edelman, C.
Sugar, M. Breuss, P. Pichler, H. Cadiou, M. Saunders, M.
Lythgoe, and J. Shaw, Clusters of iron-rich cells in the
upper beak of pigeons are macrophages not
magnetosensitive neurons, Nature, vol. 484, no. 7394, pp.
367–370, April 2012.
206 K.J. Gaston, J. Bennie, T.W. Davies, and J. Hopkins, “The
ecological impacts of nighttime light pollution:
A mechanistic appraisal,”Biol. Rev., vol. 88, no. 4, pp. 912–
927, 2013.
207 P.L. Munday et al., “Ocean acidification impairs
olfactory discrimination and homing ability of a
marine fish,”Proc. Natl. Acad. Sci., vol. 106, no. 6,
pp. 1848–1852, 2009.
208 Z. Li, F. Courchamp, and D.T. Blumstein, “Pigeons home
faster through polluted air,”Sci. Rep., vol. 6, 2016.
References 1709