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True navigation in birds: from quantum physics to global migration
Richard A. Holland
School of Biological Sciences, Queen’s University of Belfast, 97 Lisburn Road, BT9 7BL,
UK.
Short title: Bird navigation
Abstract
Birds are capable of true navigation, the ability to return to a known goal from place they have
never visited before. This is demonstrated most spectacularly during the vast migratory journeys
made by these animals year after year often between continents and occasionally global in
nature. However, it remains one of the great unanswered questions in science, despite more than
50 years of research in this field. Nevertheless, the study of true navigation in birds has made
significant advances in the previous 20 years, in part thanks to the integration of many
disciplines outside its root in behavioural biology, to address questions of neurobiology,
molecular aspects and the physics of sensory systems and environmental cues involved in bird
navigation, often involving quantum physics. However, true navigation remains a controversial
field, with many conflicting and confusing results making interpretation difficult, particularly for
those outside or new to the field. Unlike many general texts on migration, which avoid
discussion of these issues, this review will present these conflicting findings and assess the state
of the field of true navigation during bird migration.
Keywords: Navigation, Migration, Orientation, Bird, Magnetoreception, Olfaction, Map
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Introduction
The apparent ability of migratory birds to make journeys of thousands of miles, crossing deserts,
oceans and mountain ranges, sometimes even circumnavigating the globe has long fascinated
both scientists and laymen alike. Fifty years of intensive research on the mechanisms and
sensory cues required have revealed much about the way birds can achieve this feat of navigation
with such precision but also leaves many open questions and the field is one that is seen as beset
with controversy over conflicting results (Alerstam, 2006). Recently, this problem was described
as a “chronic disease” (Mouritsen and Hore, 2012), suggesting that the field is unhealthy, in a
scientific sense, and data should not be trusted. The “mystery” of how birds navigate continues
to be alluded to both in popular and professional media (Baker, 1984, HollandThorup and
Wikelski, 2007), and remains one of the great unanswered questions in science (Kennedy and
Norman, 2005) but in the last 20 years animal navigation has taken huge strides forwards by
becoming a truly interdisciplinary field. Researchers from physical, chemical, histological,
neuropysiological and electrophysiological disciplines all contribute to our understanding of bird
navigation and a researcher working in this field must now cast their literature search far wider
than the traditional behaviour focused journals that the early work was published in. This
combination of a difficulty in interpreting conflicting results and the diverse fields which
contribute to our understanding of bird navigation may make a daunting prospect for those new
to the subject. It is thus the aim of this review to assess these conflicting results and integrate the
new information from other disciplines from the perspective of a behavioural biologist working
at the level of the organism, in order to make the field more accessible to new scientists entering
the field from this area, and while remaining critical, present a positive outlook for the field of
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bird navigation. Finally, it will identify the key questions that remain in true navigation in birds
that must be tackled if the subject is to be resolved.
Migratory true navigation
What is true navigation?
Donald Griffin was the first to conceptualise bird navigation (Griffin, 1952) and he recognised a
specific form of navigational challenge, which he defined “type III”, in which the bird was able
to return to a goal after being displaced (even artificially) to an unknown area. Subsequently the
term “true navigation” was adopted to describe this by Keeton (Keeton, 1974), although Keeton
used it as a term to describe all forms of orientation and navigation from unfamiliar area that
were not explained by other processes. This was problematic as true navigation was defined by
that which could not be explained by other means, rather than as a testable hypothesis (Wiltschko
and Wiltschko, 2003). However, over time a workable hypothesis for true navigation emerged as
a number of consistent definitions acknowledged true navigation to be the ability to return to a
known goal using only cues detected locally, not by cues detected during the displacement e.g.
(Able, 2001, Phillips, 1996, Papi, 1992, PhillipsSchmidt-Koenig and Muheim, 2006). The most
current definition of true navigation is “the ability of an animal to return to its original location
after displacement to a site in unfamiliar territory, without access to familiar landmarks, goal
emanating cues, or information about the displacement route” (Phillips et al., 2006). This
definition does not specifically recognise migratory navigation however, in which the displaced
animal may not be navigating to its original location prior to displacement (i.e. homing) but a
final breeding or wintering area that it did not set out from. Hereafter this is defined as migratory
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true navigation: the ability of an animal to navigate to a specific breeding or wintering area (that
it has not just set out from) following displacement.
Evidence for migratory true navigation
Initially, a series of displacement experiments on migrating birds using mark/recapture
techniques gathered evidence for true navigation (reviewed in (Thorup and Holland, 2009)). The
clearest example (Perdeck, 1958) demonstrated that adult but not juvenile birds are capable of
migratory true navigation. More recent studies have shown that adult, but not juvenile white
crowned sparrows are able to head towards their winter area within the first 100km of departure
from the site of displacement of 3700km from their normal route during autumn migration
(Thorup et al., 2007), and that reed warblers can correct for displacements of 1000km during
their first return migrating to their previous natal area (ChernetsovKishkinev and Mouritsen,
2008). Migratory true navigation is thus experience based, i.e. an ability to correct and return to a
known goal from an unfamiliar place is a consequence of information learned on a previous
journey to, or from that goal (figure 1). The test of true navigation is thus being able to correct
after displacement to a novel location. A few studies suggest that juvenile birds may in some
circumstances appear to make corrections for displacements (Thorup et al., 2011, Thorup and
Rabøl, 2007, Thorup and Rabøl, 2001, Åkesson et al., 2005), but it is not clear whether this is the
result of homing to a known goal along the migratory route (e.g. the last known stopover site or
the natal area) or part of an inherited programme that allows them to compensate for
displacements. Such a mechanism has been described in sea turtles (Putman et al., 2011), but it
remains to be seen whether either of these mechanisms exist, or the more common viewpoint of
an inherited compass direction is the only mechanism juveniles possess.
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What is less often cited are the failures of displaced birds to correct for a displacement.
For instance, a repeat of Perdeck’s study in which adult birds were displaced to Spain did not
indicate that the birds could correct their orientation and return to the species winter area
(Perdeck, 1967). White and Golden crowned sparrows (Zonotrichia leucophrys gambelii and Z.
altricapila) that were translocated from the USA to Korea from their winter grounds did not
appear to return to the USA (MewaldtCowley and Won, 1973). The fact that some birds make
vast migrations that are global in nature is often used to argue that true navigation ability must
also be global (Bingman and Cheng, 2006), but these studies suggest that there may be limits to
the extent of a migratory true navigation ability at least in the animals studied. Whether
migratory true navigation ability varies with migration distance, or has a general limit in all birds
is not yet known, but current evidence does suggest variation, with the results of Thorup et al.
(2007) indicating at least a 3700km range, while it appears shorter in Starlings, possibly in the
region of 2000km (Perdeck, 1967).
The theory of migratory true navigation.
As the previous paragraph demonstrates, displacement experiments provide evidence for true
navigation ability, but not for how they achieve it. Although not developed to describe migratory
true navigation specifically, the “map and compass” hypothesis was developed by Kramer to
explain navigation behaviour by a process that comprises 2 steps, determining position with
respect to the goal, “the map step” and determining direction to a goal, “the compass step”
(Kramer, 1953). The map and compass theory has remained the most robust explanation for
animal true navigation since its inception and no significant challenge to the idea that animal
navigation is a two-step process has been made. True navigation ability refers specifically to the
“map” step, the ability to locate position with respect to a goal. Experienced birds are presumed
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to possess a “navigational map” that allows them to locate their position with respect to a final
goal and navigate towards it using their compass sense. One theory proposed that the map might
work in a way akin to our Cartesian coordinate system, with animals able to refer to
environmental gradients that vary predictably with latitude and longitude (figure 2). For these
gradients to be usable, the animal would have to learn that they vary predictably in intensity with
space (and possibly time) within their home range and extrapolate this beyond the learned area
(Wallraff, 1991, Wallraff, 1974). Thus when displaced to an unfamiliar area the animal could
recognise a value in the gradients that was, for example, higher than the home range and
recognise its displacement relative to it. For a migratory bird, the presumption is that this process
of learning these values occurs before departing on the first migration for the breeding area, and
during the first winter for the winter area. Thus, migratory birds are presumed to learn the value
of gradients at 2 goals. This gradient map tends to be thought of as a 2 cue system, often
presuming that a different environmental cue provides the longitude and latitude equivalents.
However, it has occasionally been suggested that different aspects of the same environmental cue
could form those two gradients (e.g. sun’s arc and sunrise time (Matthews, 1953), intensity and
slope or inclination of the magnetic field (Walker, 1998, BoströmÅkesson and Alerstam, 2012)).
Thus, we know that migratory birds can perform true navigation, and we have a theoretical
construct for how they could achieve this, but how do we study the nature of the environmental
cues and sensory systems required to achieve true navigation?
Studying migratory true navigation
The study of true navigation requires either displacement of the animal outside its familiar area,
or a simulated displacement where an environmental cue is manipulated to represent a different
location than the one currently experienced. The former requires the ability to study the response
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to the displacement in the field, and the latter requires that the animal shows behaviour in the
laboratory that correlates with orientation decisions in the wild. First, a laboratory based
correlate of migratory orientation exists in the form of migratory restlessness (Emlen and Emlen,
1966). This has been used with great success to investigate the nature of the magnetic compass
sense in migrants (Wiltschko and Wiltschko, 1972, Ritz et al., 2004, Wiltschko et al., 1993,
Zapka et al., 2009). Orientation cages provide the potential for greater control as they can be
performed indoors. Surprisingly, orientation cage studies have not been used as extensively to
investigate the cues used in the navigational map as they have the compass, despite the fact that
testing orientation after displacement has been shown to be possible (Thorup and Rabøl, 2007,
Chernetsov et al., 2008) as are simulated displacement experiments (Fransson et al., 2001,
Henshaw et al., 2010, DeutchlanderPhillips and Munro, 2012). Second, recently there have been
calls for a return to field based study of true navigation in migratory birds (Guilford et al., 2011,
Thorup et al., 2010, Wikelski et al., 2007). This stems from concerns that migratory restlessness
does not fully represent the behaviour of animals in the wild (Wikelski et al., 2007), and that we
do not understand the full extent of the challenges that animals face during migration (Holland et
al., 2007). Animal movements in the wild can now be tracked using remote monitoring devices
that provide the precision that was lacking in mark recapture techniques. In some cases GPS
precision is available and remote download from a satellite can be achieved (see (Bridge et al.,
2011) for review of currently available technology for tracking migratory birds). However,
tracking devices that can follow a migratory journey with sufficient precision to test navigational
decisions are still too large for the small songbirds that remain the focus of much of true
navigation in migration. As tracking of migratory birds becomes more widespread, our
understanding of the navigational challenges faced by both adults and juveniles will increase
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which will undoubtedly aid in adapting the theories of true navigation (Guilford et al., 2011).
However, field based study of wild birds faces the same inherent weaknesses as field based study
in the other model systems, in that control of access to cues is difficult. Field based study of
migration faces the added difficulty of predicting both the timing of departure and goal of the
animals. The former may cause problems in predicting the effect of treatments of sensory
systems particularly when they are transitory and the latter may increase the scatter in
experimental groups, meaning an increase in the number of animals needed. Given that tracking
technology remains relatively expensive and studies are often restricted by the number of devices
available, this may lead to inconsistencies in results through lack of statistical power. Such
studies are thus relatively rare, with no study of migratory true navigation using GPS telemetry
having yet been published. The field thus relies on two imperfect systems, a laboratory correlate
that provides precision and control, but which has limits in its relevance to natural behaviour,
and a field based system that is logistically difficult and lacks sufficient power at present.
The role of environmental cues in true navigation
The sensory basis of the true navigation map contributes significantly to bird navigation’s
reputation as a controversial field. Many general reviews of migration that include a chapter on
navigation avoid discussion of this sub-topic altogether (e.g. (Newton, 2007, Dingle, 1996)).
Repeatability continues to dog the field and certainly, interpreting findings where no effect of a
treatment is obtained is problematic. However, simply ignoring the large amount of research that
has attempted to elucidate the sensory basis of true navigation does a disservice to the field.
Without an understanding of research that has attempted to understand this, advances cannot be
made. The remainder of this review will thus assess the experimental evidence for sensory cues
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in migratory bird navigation, in the hope that understanding what has been tried, what has failed
and what is incomplete will aid in moving towards a resolution for this field.
Celestial cues
It has been proposed that animals could use celestial cues for navigation (Matthews, 1953,
Matthews, 1951, Pennycuick, 1960). Both the sun and stars can provide a cue to north-south
position because the zenith varies with latitude. Longitudinal displacement could potentially be
detected if they were able to recognise that sun or star rise time was different from that at the
goal site. What is more, these provide a global reference frame and so in theory the animal’s
position could be located anywhere on the Earth so long as a view of the cue was available.
However, both sun and star navigation are generally rejected based on two factors. First, tests on
homing pigeons have demonstrated that they have a time compensated sun compass that can be
manipulated by shifting their internal clock (Schmidt-KoenigGanzhorn and Ranvaud, 1991,
Schmidt-Koenig, 1960). This rejects sun navigation on two counts. First, it suggests that the
birds (or at least homing pigeons) do not note the altitude of the sun, or they would not be fooled
by the shifts in their internal clock and thus do not use it as a cue to latitude. Second, a 6 hour
forward shift in the internal clock leads to a deflection of approximately 90° counter clockwise
(i.e. to the west), matching the rate of movement of the sun across the sky. This is not consistent
with the use of the sun as a cue to longitude, which would be perceived as a displacement of
approximately 5000km to the west (i.e. the bird would need to fly east to return home). It has
been argued that such displacements are unrealistic to a homing pigeon, and so a six hour shift is
an unrealistic test of the sun navigation hypothesis (Pennycuick, 1961). However, subsequent
tests involving much smaller shifts were also consistent with sun compass but not sun navigation
(Walcott and Michener, 1971). On this basis sun navigation has been rejected (Baker, 1984).
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Clock shift has also been demonstrated in migratory birds in orientation cages, which might
suggest it should be rejected for migratory true navigation (Able and Cherry, 1986, Able and
Dillon, 1977, Muheim and Akesson, 2002), and one study did not support a significant role for
either the sun compass or sun navigation in a migrant songbird (Munro and Wiltschko, 1993).
The original experiments of Emlen, which established stars as a compass cue , actually
provided some suggestion of time compensation, although only with three birds (Emlen, 1967).
However, subsequent investigation provided no evidence of time compensation (Mouritsen and
Larsen, 2001), without which longitude is not discernible. Additionally, there is no evidence for
a clock mechanism playing a role in detecting displacements per se, which would preclude both
star and sun navigation as a mechanism for longitude (KishkinevChernetsov and Mouritsen,
2010). However, a meta-analysis of displacement experiments of juvenile migratory birds in
orientation cages suggests that they are more likely to correct under starry skies than overcast
skies, suggesting a role for celestial cues in this behaviour (Thorup and Rabøl, 2007). Indeed,
many studies of the role of sun and stars in migratory navigation test only juvenile birds (e.g.
Mouritsen and Larsen 2001, Muheim and Akesson 2002), or the age is not reported (e.g. Able
and Dillon 1977, Able and Cherry 1986). Rejection of celestial navigation thus relies to some
extent on the assumption that the cues used by homing pigeons and migratory birds are the same.
It is however difficult to reconcile the global availability of celestial navigation with the apparent
limits on true navigation in some migrating songbirds (see above).
Infrasound
Sounds in the range of 0.1-10 Hz are known to spread over hundreds if not thousands of miles. If
stable, these have the potential to act as a gradient for navigation. Evidence has been presented
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that pigeon homing performance is disrupted by infrasound disturbance, such as disturbance of
pigeon races by sonic booms of aircraft (Hagstrum, 2000, Hagstrum, 2001), or fluctuations in
orientation performance that correlate with atmospheric fluctuations (Hagstrum, 2013). The data,
while in many cases compelling, are correlational however, making it difficult to currently assess
whether this is a result of disruption of infrasound navigation cues, co-correlation with other
factors propagated by atmospheric means, or disturbance in motivation to home. An experiment
which removed the cochlea of homing pigeons did not produce any deficits in homing
performance (Wallraff, 1972), which, although not precluding that infrasound is part of a
multifactorial map, does not support the argument made by (Hagstrum, 2013) that infrasonic
cues are the sole solution to the navigational map question in pigeons. No experiment has yet
demonstrated any effects of infrasound on bird migration. Nevertheless, it remains a viable cue
which should be investigated further and the range over which it could operate makes it a
possibility for the distances seen in migratory displacements.
Olfactory cues
No aspect of bird navigation contributes to its reputation as a controversial field more than that
of the role of olfactory cues in the true navigation map. By far the majority of work has involved
homing pigeons and a large number of experiments, possibly more than in any other aspect of
bird true navigation, have been performed. A comprehensive review of these experiments is
available in (Wallraff, 2005) and a detailed treatment of all of these is beyond the scope of this
review given that the focus is on navigation in migratory birds,. However, olfactory navigation is
the most extensively tested hypothesis in true navigation and as such its potential role in true
navigation of migrants should be considered.
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Key findings in olfactory navigation
Olfactory deprivation removes the ability of homing pigeons to return to the home loft, and this
is most clearly demonstrated by sectioning the olfactory nerve (Gagliardo et al., 2006, Gagliardo
et al., 2008, Gagliardo et al., 2009, Benvenuti et al., 1973). Further key findings in which
orientation is altered rather than impaired have been argued to suggest that the olfactory cues
provide navigational information to homing pigeons. A ‘false release site’ experiments in which
birds were transported to a releases site in one direction, allowed to sample air from this site, and
then transported to a release site in the opposite direction without further access to environmental
odours found that birds flew in the direction expected if they were trying to home from the
original release site (Benvenuti and Wallraff, 1985). An experiment in which artificial odours
(benzaldehyde) were presented to pigeons at the loft from the north west by fans found that when
displaced with benzaldehyde on their beaks, the birds oriented in the direction consistent with a
north west displacement, rather than with the actual home direction (IoaleNozzolini and Papi,
1990). Further experiments in which lofts are shielded or winds are manipulated argued that
pigeons learn to associate odours brought by different wind directions with different directions
(Baldaccini et al., 1975, Ioale et al., 1978, FoaBagnoli and Giongo, 1986, Gagliardo et al., 2001).
In theory this does not require sampling of gradients as suggested by the bi-coordinate map, but
merely association between an odour and a direction.
Criticisms of olfactory navigation
Olfactory navigation has been criticised on a number of counts. First, lack of repeatability of the
effects of olfactory deprivation argues that olfaction is neither the only, nor an essential cue
(Wiltschko, 1996). However, it is not clear whether this lack of repeatability comes from
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redundancy in navigation cues or from variations caused by difficulties in control of the field
based system of experimentation, or in the experiments themselves. If homing performance of
birds treated with zinc sulphate is considered, olfactory deprivation has been demonstrated in a
number of countries and on four continents (Wallraff, 2005). A number of the key findings have
also been challenged. The deflector loft effect is shown in some cases to be a consequence of
deflection of polarized light, involved in compass calibration, as anosmic birds still deflect after
exposure (Phillips and Waldvogel, 1982, Waldvogel and Phillips, 1991, WaldvogelPhillips and
Brown, 1988). However, the similar findings of experiments in which winds are reversed or
shielded are not challenged by this discovery. The question of whether olfactory inputs are
navigational or related to motivational factors has always been a concern in interpretation
(Wiltschko, 1996). In support of this odours appear to ‘activate’ other navigational processes in
young pigeons navigating by route reversal (JorgeMarques and Phillips, 2009). Jorge et al. found
that young pigeons, which navigate by route reversal, were unable to orient homeward if
transported in filtered air, but could if transported either with access to natural odours, or
artificial ‘novel’ odours. This argues that smelling ‘non-home’ odours I, triggers the bird to
access a navigation system based on other cues. The site simulation experiments of Benvenuti
and Wallraff (1985) have also been argued to be a consequence of activation of a navigational
map by non-navigational olfactory cues rather than navigational in themselves (JorgeMarques
and Phillips, 2010). Presenting non-specific odours at the false release site produced the same
behaviour as access to natural odours. A subsequent test of the activation hypothesis did not
support a role for activation however, birds transported to a release site with access to novel
odours were no more likely to orient homewards than those transported in filtered air (Gagliardo
et al., 2011). However, they used higher concentrations of novel odours than those used in the
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previous navigation experiments, which it has been argued would make the pigeons anosmic
(Phillips, personal communication). However, the experiments of (Ioale et al., 1990) cannot be
explained by activation, as if the benzaldehyde odour was activating a non-olfactory navigational
map, it would result in homeward orientation, not orientation consistent with a north west
displacement. One striking finding of the experiments on olfactory navigation in pigeons is that
if olfactory navigation is correct generally, it suggests that the view of redundancy of cues is not
correct. Where olfactory deprevation effects have been demonstrated they lead to significant
impairment of homing performance of pigeons at unfamiliar release sites, i.e. the majority do not
return to the home loft. If olfactory cues are navigational, this argues that in their absence no
cues are available to take their place which goes against the widely held view that the
navigational map must be made up of redundant cues (Walcott, 1996, Wiltschko et al., 2010).
Olfactory navigation thus continues to provide debate and has not been widely accepted as an
explanation for true navigation in homing pigeons.
While the olfactory navigation hypothesis is by far the most extensively tested when
considering pigeon homing, it has rarely been considered when discussing true navigation in
migrating birds. Stable odour gradients such as would be necessary for a bi-coordinate map have
not been demonstrated to exist beyond approximately 200km (Wallraff and Andreae, 2000). This
makes it difficult to explain the majority of displacement experiments on migrants by the use of
olfactory navigation. Nevertheless, two experiments on homing of migratory birds in the
breeding season found a deficit in performance after olfactory deprivation (Wallraff et al., 1995,
FiaschiFarina and Ioalé, 1974). More surprisingly, a recent experiment demonstrated that adult
catbirds displaced 1000km east from Illinois to Princeton in the USA, subjected to olfactory
deprivation by zinc sulphate treatment and then radio-tracked from a light aircraft were unable to
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correct for the displacement in the way that controls were (Holland et al., 2009). If this finding is
borne out by further experimental support and shown to be a deficit based on removal of
navigation cues, then it may require a re-analysis of the bi-coordinate map theory for true
navigation. It appears to be hard to explain how stable olfactory gradients could exist over the
1000km necessary to explain this behaviour navigationally. Homing pigeons have not been
shown to use olfactory cues beyond 700km, and then only if they had access to environmental air
during the displacement (Wallraff, 1981).
With regard to the use of olfactory signals by migrants, an interesting parallel finding
from a neurobiological study of migratory restlessness is that both visual and olfactory areas of
the brain become more active at night during the migratory period, while they are most active
during the day outside this time (Rastogi et al., 2011). This suggests that olfaction plays a
significant role in migratory behaviour, but it is still an open question as to what role this is. A
recent hypothesis proposes that in fact the primary role of olfaction across organisms (and thus
reason for its evolution) is navigation (Jacobs, 2012). If it does indeed turn out to be the case
then theories of true navigation based on a bi-coordinate map made stable environmental
gradients may need to be significantly reconsidered, since olfactory cues do not seem to fit easily
into this paradigm.
Magnetic cues
The intensity of the Earth’s magnetic field was proposed as a cue for bird navigation over a
century ago (Viguier, 1882). The Earth’s magnetic field is stronger at the poles than at the
equator and it therefore has the potential to indicate latitudinal position. However, this is only
functional over a relatively coarse scale (Bingman and Cheng, 2006).There are variations in the
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strength of the magnetic field at a fine scale that mean it may be stronger at a lower latitudes in
some cases and varies with longitude rather than latitude in some places (Phillips et al., 2006).
Thus, even at a coarse scale the magnetic field may not be as consistent a cue to latitudinal
position as it is often portrayed. In seeming support of this, a number of experiments in which
magnets are attached to the heads of birds homing over long distance failed to find any deficit in
homing performance (BenhamouBonadonna and Jouventin, 2003, Bonadonna et al., 2005,
Mouritsen et al., 2003). However, since the 1960’s evidence of behavioural responses to
artificially changing the Earth’s magnetic field have been obtained (Merkel and Wiltschko, 1965,
Wiltschko and Wiltschko, 1972). To date at least 24 species of bird have been shown to respond
to changes in the Earth’s magnetic field (Wiltschko and Wiltchko, 2007) but by far the majority
of studies on magnetoreception in birds involve investigating its use as a compass and it has been
challenging to demonstrate the use of the magnetic field for a map (Phillips et al., 2006).
Artificial displacement experiments, where the magnetic field is changed to indicate different
latitudes to birds orienting in emlen funnels, provide some support that birds recognise magnetic
intensity signatures as a cue to end migration (Henshaw et al., 2010, FischerMunro and Phillips,
2003). However, in these studies (performed on Silvereyes, Zosterops l. lateralis and Lesser
Whitethroats Sylvia curruca) intensity signatures indicating displacements outside of the normal
range and migration route of the population did not produce navigational responses, as would be
expected for a map cue. Instead they become disoriented. This may be a similar response to that
seen in juvenile migrants, in which magnetic “sign posts” indicate latitudes at which innate
compass directions must change for successful migration (Beck and Wiltschko, 1988) and thus
the birds may merely stop migrating when a certain latitude is reached. Interestingly, this is also
consistent with activation, as proposed for olfactory cues, with magnetic field signatures
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activating a non-magnetic navigation system below some threshold value, but once that value is
reached, the navigation system is no longer activated, even if the magnetic value is far greater
than the threshold. A recent follow-up study has indicated that only adults are affected by such
magnetic displacements suggesting that it is a different behaviour than the innate signpost
recognition seen in juveniles (Deutchlander et al., 2012). However, the lack of orientation
towards the winter site when the artificial displacement was north of it remained, making it
difficult to conclude that the behaviour represented true navigation in the strict sense rather than
an age dependant response to latitudinal sign posts, or activation of other navigational cues.
Recall however, that when (Perdeck, 1958) displaced adult starlings outside the wintering
latitude, they were able to correct and return to the normal winter area. This indicates the
challenge of orientation experiments: it is possible that different site fidelity is present in the
different species tested, with starlings showing more fidelity to their winter site than Silvereyes
or Lesser Whitethroats, and thus these two species do not represent the ideal model for this test.
Contrast this to similar experiments on newts, turtles and spiny lobsters, which have been
demonstrated to alter their orientation in response to artificial displacements either north or south
of their current position (Fischer et al., 2001, Lohmann et al., 2004, Lohmann et al., 1995).
Experiments on the orientation performance of homing pigeons has also been shown to be
disrupted at magnetic anomalies (areas with stronger or weaker magnetic intensity than
expected), which suggests that magnetic intensity plays a role in their navigational map
(DennisRayner and Walker, 2007, Walcott, 1991, Wiltschko et al., 2010, Mora and Walker,
2009), although many of these experiments are conducted within a range where the variation in
magnetic intensity is thought to make the earth’s magnetic field unreliable as a cue to position
(Phillips et al., 2006). This may indicate a different mechanism than that proposed for true
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navigation in migrating birds, or perhaps that magnetic intensity correlates with other factors
which disrupt orientation in these experiments (Wallraff, 2005). Part of the challenge in
demonstrating a role for magnetic intensity has been because most navigational experiments
involve sensory manipulation, and the way in which birds sense the magnetic field is by far the
most uncertain aspect of navigation research. However, within the last 20 years, significant
advances have been made in this area. This has involved the integration of theoretical work from
physics, biochemistry, neurobiology and molecular biology alongside traditional behavioural
experiments. As a consequence, we now have an understanding of the way birds may perceive
aspects of the magnetic field and how this may contribute to the map and the compass aspects of
true navigation. An understanding of the potential sensory pathways is thus crucial to
understanding the behavioural experiments that support the use of the magnetic field as a map.
The magnetic sense: different receptors for different tasks?
The behavioural evidence for magnetoreception was met with initial scepticism due to the lack of
an obvious sense organ. However, consideration of physical principles of the magnetic field
means that such sense organs need not be located at the surface in the same way as photo or
auditory receptors must: the Earth’s magnetic field can pervade all tissue. During the 1980’s
several models were proposed for magnetoreception but 2 have withstood scrutiny: a mechanism
based on photoreceptive molecules (the radical pair mechanism) and a mechanism based on
magnetic iron particles (the ferrimagnetic mechanism).
Radical pairs
Magnetically sensitive reactions involve radicals in which unpaired electrons are present in
different “spin” states, either antiparallel (“singlet” state) or parallel (“triplet” state) (Rogers and
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Hore, 2009). The yield of the different states has been demonstrated to be influenced by strong
magnetic fields, and based on this it was hypothesised that a molecule that formed such radicals
in different yields depending on the magnetic field alignment could be the basis of a
magnetoreceptor (SchultenSwenberg and Weller, 1978) (figure 3). It was subsequently
discovered that magnetic compass orientation is dependent on the wavelength of light (Wiltschko
et al., 1993, Wiltschko and Wiltschko, 2006) and so the model was modified to suggest that the
molecule involved in the radical pair process was photoreceptive and that a photon of light
would instigate this reaction (RitzAdem and Schulten, 2000). Evidence that the magnetic
compass was lateralized via the right eye to the left brain hemisphere suggested that the magnetic
field was perceived through the eyes (Wiltschko et al., 2002b), although see (Hein et al., 2011)
for evidence of no lateralization. A study involving ZENK, an immediate early gene which is
expressed in neurones indicated that an area of the brain called cluster-N, responsible for night
vision was active during migratory restlessness (Mouritsen et al., 2005). A subsequent study in
which this area of the brain was lesioned indicated that migratory robins could no longer use
their magnetic compass (Zapka et al., 2009). Thus, migratory songbirds appear to possess a
magnetoreceptor mediated by the visual system which is based on a photoreceptive molecule.
Evidence that this is because of a radical pair mechanism comes from an experiment based on
the prediction that the interaction between a radical pair and the magnetic field could be
disrupted by a weak electromagnetic field in the radio spectrum (1.315 MHz, the so called
Larmor frequency). It was indeed the case that migratory robins could no longer orient in an
emlen funnel when such a field was applied (Ritz et al., 2004). The molecule involved has been
proposed to be a cryptochrome (Ritz et al., 2000). This is a blue light receptor and appears to
form long lived radical pairs, which would be necessary for it to work as a magnetoreceptor
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(Liedvogel et al., 2007). Four different cryptochromes have been found in the eyes of migratory
birds, Cry 1a, (Mouritsen et al., 2004, Moller et al., 2004, Niessner et al., 2011), Cry 1b (Moller
et al., 2004), Cry 2 (Mouritsen et al., 2004) and Cry 4 (Mouritsen et al., 2004). In terms of figure
3, it is thought that the radical pair comprises a flavosemiquinone radical and a terminal residue
of a conserved triad of tryptophan residues (a flavin-tryptophan radical pair) (Maeda et al., 2012,
Biskup et al., 2009). Based on our understanding of how a similar reaction occurs in plants, the
flavosemiquinone radical would appear to lead to the signalling state (Bouly et al., 2007). No
direct evidence yet exists however, to demonstrate that cryptochrome is the primary sensing
molecule involved in magnetoreception (Mouritsen and Hore, 2012, Liedvogel and Mouritsen,
2010). More detailed discussion of the issues around the radical pair compass can be found in
(Mouritsen and Hore, 2012, Rogers and Hore, 2009). What is crucial to this review is, does it
have a role in the navigational map? All the experiments described above involved disrupting the
magnetic compass, in no case was there an indication that the radical pair pathway is involved in
map navigation. It does not appear that this mechanism detects intensity, nor indeed the polarity
of the magnetic field, only inclination (Ritz et al., 2000). In theory, inclination could be used to
detect latitude, so there is no reason why the radical pair mechanism could not be involved in the
navigational map, but no experiment has tested this hypothesis. This may be because it could be
challenging to design an experiment that is able to disentangle the use of the radical pair sense
for a compass from its use in a map.
The Ferrimagnetic sense
Ferrimagnetic materials are those in which spontaneous magnetization occurs because the
magnetic moments of atoms are opposed but unequal. This is seen in iron oxides, including the
oldest known magnetic substance, magnetite. Ferrimagnetic material exists in a number of
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crystalline “domains”, including multi, single and supaparamagnetic. Multi domain magnetite
has no magnetisation, single domain has a permanent magnetic moment whereas
superparamagnetic magnetite has a fluctuating magnetic moment, but it can be aligned to an
external magnetic field (Kirschvink and Walker, 1985). Based on the discovery that bacteria
containing single domain magnetite passively align to the magnetic field (Blakemore, 1975), and
that magnetite is a biogenic material that is present widely in the tissue of a diverse array of
organisms, it was proposed that such material could form the basis of a magnetic sense in multi-
cellular organisms (Kirschvink and Gould, 1981, Yorke, 1979). To test this, it was proposed that
the physical properties of the ferrimagnetic material could be used to predict the presence of
magnetic material in sensory cells in the same way as it had been done in bacteria (Kirschvink,
1982). If ferrimagnetic material was involved in a sensory receptor that detected the Earth’s
magnetic field then a brief strong magnetic pulse that exceeded the coercivity (the magnetic
force required to reduce the magnetisation of the substance to zero) would re-magnetise the
substance in the opposite direction if applied antiparallel to the original magnetization (Figure 4).
For most biogenic magnetite, the strength required to re-magnetise would be 0.1T, 5000 times
the strength of the Earth’s magnetic field (Kirschvink et al., 1985). If single domain magnetite
was present it would be re-magnetised, and if used by sensory cells, in theory, would lead to a
change in the information the receptor gave. Subsequently, a significant number of experiments
have treated birds, with a strong magnetic pulse and indeed found that their orientation is
affected by such a pulse. Effects have been found both on migratory birds tested in emlen
funnels (BeasonDussourd and Deutschlander, 1995, Wiltschko and Wiltschko, 1995, Wiltschko
et al., 1994, Wiltschko et al., 1998), in naturally migrating birds (Holland, 2010) and in homing
pigeons (BeasonWiltschko and Wiltschko, 1997). In all these cases a magnetic pulse leads to a
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deflection in orientation. However, where the pulse was applied antiparallel to the direction of
magnetisation, the expected reorientation in the opposite direction did not occur (Wiltschko et
al., 2002a, Holland, 2010). This is not consistent with single domain magnetite that is free to
rotate in the way a bacteria cell can and does not fit with the popularized concept of a
ferrimagnetic sense consisting of tiny compass needles (Mouritsen, 2012). Nor is the fact that the
pulse effect appears to be temporary, with birds returning to normal orientation after
approximately 10 days (Wiltschko et al., 2007, Wiltschko et al., 1998). This does not support the
permanent re-magnetisation of magnetic material. One pulse experiment demonstrated that the
deflecting effect of the pulse was removed if the ophthalmic branch of the trigeminal nerve
(which innervates the beak) was anaesthetised with lidocane, a local anaesthetic (Beason and
Semm, 1996). This suggested that the magnetic pulse effected receptors located in the beak area
and the trigeminal nerve was responsible for conveying the input from these receptors to the
brain.
Two subsequent studies have confirmed the finding that the trigeminal nerve conveys
magnetic information. Mora and colleagues (Mora et al., 2004) conditioned homing pigeons to a
magnetic intensity anomaly, and found that they could no longer discriminate if the trigeminal
nerve was lesioned (although see (KirschvinkWinklhofer and Walker, 2010) for possible
weaknesses in the experimental design and (KishkinevMouritsen and Mora, 2012) for failure to
repeat the conditioning paradigm). This indicated that the trigeminal nerve was responsible for
conveying information on the magnetic field. Following this a study of ZENK expression
indicated activation of neurons in the trigeminal brainstem only in migratory robins orienting in a
magnetic field that had an intact trigeminal nerve (Heyers et al., 2010). However, homing
pigeons that had their trigeminal nerve lesioned were not disrupted in their homing performance
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(Gagliardo et al., 2006, Gagliardo et al., 2008, Gagliardo et al., 2009). Until recently this made
the study of Beason and Semm (1996) the only study to date to indicate a role for the trigeminal
nerve in the process of navigation, but what aspect of navigation? Lesions of the trigeminal nerve
do not appear to affect magnetic compass orientation in juvenile robins (Zapka et al., 2009), and
the pulse deflects the orientation of birds in emlen funnels, but does not affect the magnetic
compass (Wiltschko et al., 2006, Munro et al., 1997b). A particular design of pulse experiment
however suggests a possible role for the ferrimagnetic receptor in bird navigation. Pulses only
appear to effect the orientation of adult migrating birds, not juveniles (Munro et al., 1997a,
Munro et al., 1997b, Holland and Helm, 2013), which suggests that the ferrimagnetic sense is
involved in an experience based mechanism possessed by adult but not juvenile birds. Since
adults have true navigation, this suggests the ferrimagnetic sense is involved in the true
navigation map. A recent study has also shown that migrating reed warblers returning to their
breeding grounds, are unable to correct for a displacement of 1000km eastwards if the trigeminal
nerve is cut, unlike intact and sham operated birds, who are able to do so (Kishkinev et al.,
2013). This finding, on migratory birds, is in contrast to the findings on homing pigeons, where
no role for the trigeminal nerve in navigation is supported.
On this basis it is argued that migrating birds possess two magnetoreceptive pathways: a
radical pair mechanism in the eye, which is responsible for at least compass orientation, and a
ferrimagnetic sense, which is implicated in the detection of magnetic intensity and is involved in
the navigational map (Wiltschko and Wiltchko, 2007). However, caution is urged in accepting
this interpretation without question. Adult but not juvenile migratory birds have been shown to
respond to changes in intensity (Deutchlander et al., 2012) and adult but not juvenile migratory
birds have been shown to be affected by a strong magnetic pulse (Munro et al., 1997a, Holland
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and Helm, 2013), but there is no direct causal link between the two. Similarly, the trigeminal
nerve has been shown to be involved in detecting the magnetic field (Mora et al., 2004), the
pulse effect no longer persists when this is anaesthetised, and migratory birds with trigeminal
nerve section can no longer correct for displacement (Kishkinev et al., 2013), but there is no
direct link between the pulse and magnetic intensity, or the trigeminal nerve and magnetic
intensity. Evidence for a ferrimagnetic sense that is responsible for detecting intensity as part of a
true navigational map is thus based on several indirect links. We do not know for certain that the
pulse affects a receptor that detects intensity, only that it changes navigation behaviour and that
the behaviour appears to be mediated by the trigeminal nerve. To be certain of that we would
need to know the nature and location of the magnetic receptor.
The ferrimagnetic receptor: magnetite or macrophage?
Initially, iron-containing cells found in the upper beak of the homing pigeons and other birds
were suggested as magnetoreceptors innervated via the trigeminal nerve, although no clear
sensory receptor was identified (Beason and Nichols, 1984, Williams and Wild, 2001). A
structure that has the potential to be a magnetic receptor has been described in the beak of
homing pigeons (Fleissner et al., 2003), chickens (Gallus domesticus), Garden Warblers (Sylvia
borin) and Robins (Erithacus rubecula) (Falkenberg et al., 2010). The structure appears to
consist of sensory dendrites in the upper beak, which contains iron rich bullets and an iron
containing vesicle. It is argued that these are distributed in such a way as to provide magnetic
field information in three axes and thus form elements of a magnetometer. Appearing to support
the argument that this is a magnetoreceptor, the effect of a magnetic pulse disappears when the
upper beak is anaesthetised with local anaesthetic (Wiltschko et al., 2009). The disrupting effect
of a magnetic anomaly on homing pigeon orientation also disappears when the beak is
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anaesthetised (Wiltschko et al., 2010). Again, however, the link is indirect. It is not certain that
the anaesthetic is acting directly on the magnetoreceptor in these experiments, and the effects of
local anaesthetics have been questioned (Mouritsen and Hore, 2012). A further significant
cautionary note to the beak based magnetoreceptor theory has recently emerged. A thorough
study made on homing pigeons (Treiber et al., 2012) strongly suggested that the majority of cells
identified as containing iron, if not all, both in the upper beak and other parts of the body, such as
the skin, respiratory epithelium and feather folliculi are macrophages, cells responsible for
engulfing waste and pathogens in the body. Treiber et al. (2012) argue that the structures
described in previous work are thus not sensory cells at all. This raises the question of whether a
magnetoreceptor exists in the beak. However, the work of Treiber et al. (2012) should not be
over interpreted. While the burden of proof is on those who argue that the beak is the site of
magnetoreception (Mouritsen, 2012), Treiber et al. do acknowledge that there may be
magnetoreceptors in some as yet unidentified location in the beak. Added to this, a number of
behavioural studies supporting magnetoreception in the beak have been identified (Wiltschko
and Wiltschko, 2013).
A second potential site of a magnetoreceptor has also been identified, in the inner ear
lagena of homing pigeons, using electrophysiology recordings (Wu and Dickman, 2011, Wu and
Dickman, 2012). Recent evidence from electron microscopy has identified iron rich cells in the
inner ear (Lauwers et al., 2013), although they do not fit all the properties of a magnetoreceptor.
Furthermore, experiments on homing pigeons did not show any deficit in homing with the inner
ear removed (Wallraff, 1972), so unlike the beak based sense, behavioural evidence is lacking.
Future perspectives: Chronic disease or rude health?
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As noted at the start of this review, a recent review of magnetoreception suggested that this field
suffered from a chronic disease in its lack of repeatability of findings (Mouritsen and Hore,
2012). It could be argued that this applies equally to all aspects of bird navigation, with many
experiments failing to repeat others, or contradictory results within and between different
disciplines. Does this mean that research on bird navigation is in ill health? The assertion by
Mouritsen and Hore that experiments must be carefully controlled and designed to avoid
observer bias is an important one. However, the recent work of Treiber et al. (2012) that
questions the structure and location of magnetoreceptors could actually be viewed as a strength
and sign of health: of a field that welcomes new results that may force revisions of current
models of understanding. While many aspects of navigation are unresolved, as this review
indicates, that does not mean that there is no data. While the models for studying navigation are
imperfect, closer links between laboratory work and field work are being established and the
addition of new technology for studying animals in the wild will broadened our understanding of
the behaviour of migrating birds and the challenges they face (Guilford et al., 2011). The
integration of neurobiology, physics and molecular biology into the discipline is now well
established and has led to a number of breakthroughs in our understanding of the magnetic sense
as well as the role of the olfactory sense in navigation. The integration of these disciplines has
led to testable predictions about the structure of sensory systems and potentially the mechanisms
of navigation. For the field to advance further, the link between these disciplines and behavioural
biology needs to strengthen further, in order to reduce the “black box” understanding of some of
the systems involved. For example, a better knowledge of the structure of the ferromagnetic
sense will allow better predictions about the effect of magnetic pulse treatments to understand
how receptors are changed by the treatment. Strengthening this integration of other disciplines,
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whilst maintaining the roots as a behavioural biology discipline, will ultimately lead to the
solution of the “mystery” of bird navigation. . I will finish this review by highlighting some of
the key issues that should be resolved in order for the field of true navigation in migratory birds
to advance
Key questions in migratory true navigation
1) Is the true navigation map unimodal, i.e. one environmental cue provides all information
on location, bimodal, i.e. two separate environmental cues provide different aspects of the
location (e.g. latitude and longitude), or redundant, i.e. do multiple cues provide the same
information for different aspects of the location. Solving this will help to understand
some of the inconsistencies and conflicting evidence in the field, as it will establish
whether failure to repeat is a consequence of experimental design rather than redundancy
of cues.
2) Are there one or two magnetic sensory systems with different functions? Clearly
establishing whether the magnetite based system is responsible for detecting intensity
would establish that not just direction but also other aspects of the magnetic field could
be used and form part of the magnetic map.
3) Related to 2), can a magnetite based sensory receptor be located and described?
Understanding the structure of the magnetoreceptor will help to provide testable
predictions for how it might control birds’ behaviour, particularly in light of the pulse
experiments.
4) To what extent does migratory behaviour in the wild mirror behaviour in an orientation
cage? The field of navigation now involves multiple disciplines including those outside
biology and requires a controlled laboratory based system that allows predictions to be
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tested by isolating cues. The orientation cage provides this. However, currently, we have
little understanding of how small songbirds respond to displacements in the wild with
current techniques being too coarse (ringing, geolocators) or lacking in range (radio
tracking). Understanding how songbirds respond to displacements in more detail will
indicate the range of their navigation system and thus the extent to which environmental
cues will provide reliable information on their location.
5) Is “activation” a significant phenomenon within true navigation? The results of some
experiments on both olfactory and magnetic cues are consistent with them activating
other navigational cues, but this would appear to violate the principle of Occam’s razor
by adding another step to the navigation process: If activation plays a part in true
navigation, then it moves from a 2 step process (what is my location, what direction to
reach home?) to a 3 step process (Am I at home? If no, what is my location, what
direction to reach home?), and the two cues providing the most evidence for navigation
(olfactory and magnetic) become relegated to intermediate steps towards the actual
navigational cues.
Acknowledgements
I thank John Phillips and two anonymous reviewers for helpful comments on the manuscript.
Aspects of this review also came as a result of enjoyable discussions with the Navigation
special interest group at the MIGRATE NSF funded meeting in Konstanz, 2010 with
Susanna Åkesson, Verner Bingman, Tim Guilford, Anna Gagliardo, Henrik Mouritsen,
Rachel Muheim, Rosie Wiltschko and Wolfgang Wiltschko.
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Figure legends
Figure 1.
Migratory true navigation (A1, A2) is distinct from homing (B) in that the goal is dependent
upon the season. If displaced during the breeding season the animal homes to the same location.
If displaced from the breeding ground during or just prior to migration, the animal will navigate
to the winter ground (A1), or if displaced from the winter ground, to the breeding ground (A2).
Whether this requires different mechanisms or cues that homing has not yet been established.
Figure 2.
In a bi-coordinate map, two gradients (represented by the broad intersecting arrows A and B) are
learned by exploration in the home breeding area. As long as the gradients continue to increase
or decrease predictably, then if a bird is displaced, it can compare the values at the displaced
location with those at the desired goal to calculate the direction of displacement. Only by
learning the values of the winter area can the bird navigate to it, and so migratory true navigation
can only be achieved by adult birds that have made a previous journey.
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Figure 3.
A simplified schematic of the radical pair reaction. A photoreceptive molecule forms radical
pairs in the presence of specific wavelengths of light. An applied magnetic field alters the yield
of conversion between singlet and triplet states (yield A vs. yield B in the diagram), leading to
different expression of the signalling state of the molecule (after (Rogers and Hore, 2009)). It has
been hypothesised that this signalling state may be expressed as patterns on the retina, thus
allowing to bird to see the magnetic field, but this has not yet been confirmed (Ritz et al., 2000) .
Figure 4.
Chains of single domain magnetite align with a biasing magnetic field in the direction of
magnetisation (indicated by the red end). Application of a strong magnetic pulse antiparallel to
the direction of magnetisation will re-magnetise in the opposite direction. If such chains are
present in sensory cells and were free to rotate they would give different information about the
magnetic field after such a treatment. In practice however, the effect of pulse treatments on birds
do not clearly indicate that such structures exist.
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