true navigation in birds: from quantum physics to global migration

R E V I E W

True navigation in birds: from quantum physics to globalmigrationR. A. Holland

School of Biological Sciences, Queen’s University of Belfast, Belfast, UK

Keywords

navigation; migration; orientation; bird;magnetoreception; olfaction; map.

Correspondence

Richard Holland, Queen’s University Belfast,School of Biological Sciences, 97 LisburnRoad, Belfast, BT9 7BL, UK.Email: [email protected]

Editor: Steven Le Comber

Received 24 June 2013; accepted 05December 2013

doi:10.1111/jzo.12107

AbstractBirds are capable of true navigation, the ability to return to a known goal from aplace they have never visited before. This is demonstrated most spectacularlyduring the vast migratory journeys made by these animals year after year, oftenbetween continents and occasionally global in nature. However, it remains one ofthe great unanswered questions in science, despite more than 50 years of researchin this field. Nevertheless, the study of true navigation in birds has made signifi-cant advances in the previous 20 years, in part thanks to the integration of manydisciplines outside its root in behavioural biology, to address questions of neuro-biology, molecular aspects, and the physics of sensory systems and environmentalcues involved in bird navigation, often involving quantum physics. However, truenavigation remains a controversial field, with many conflicting and confusingresults making interpretation difficult, particularly for those outside or new to thefield. Unlike many general texts on migration, which avoid discussion of theseissues, this review will present these conflicting findings and assess the state of thefield of true navigation during bird migration.

Introduction

The apparent ability of migratory birds to make journeys ofthousands of miles, crossing deserts, oceans and mountainranges, sometimes even circumnavigating the globe, has longfascinated both scientists and laymen alike. Fifty years ofintensive research on the mechanisms and sensory cuesrequired have revealed much about the way birds can achievethis feat of navigation with such precision, but also leavesmany open questions, and the field is one that is seen as besetwith controversy over conflicting results (Alerstam, 2006).Recently, this problem was described as a ‘chronic disease’(Mouritsen & Hore, 2012), suggesting that the field isunhealthy, in a scientific sense, and data should not be trusted.The ‘mystery’ of how birds navigate continues to be alludedto both in popular and professional media (Baker, 1984;Holland, Thorup & Wikelski, 2007), and remains one of thegreat unanswered questions in science (Kennedy & Norman,2005), but in the last 20 years, bird navigation has takenhuge strides forwards by becoming a truly interdisciplinaryfield. Researchers from physical, chemical, histological,neuropysiological and electrophysiological disciplines all con-tribute to our understanding of bird navigation, and aresearcher working in this field must now cast their literaturesearch far wider than the traditional behaviour-focused jour-nals that the early work was published in. This combination ofa difficulty in interpreting conflicting results and the diverse

fields that contribute to our understanding of bird navigationmay make a daunting prospect for those new to the subject. Itis thus the aim of this review to assess these conflicting resultsand integrate the new information from other disciplines fromthe perspective of a behavioural biologist working at the levelof the organism, in order to make the field more accessible tonew scientists entering the field from this area, and whileremaining critical, present a positive outlook for the field ofbird navigation. Finally, it will identify the key questions thatremain in true navigation in birds that must be tackled if thesubject is to be resolved.

Migratory true navigation

What is true navigation?

Donald Griffin was the first to conceptualize bird navigation(Griffin, 1952), and he recognized a specific form of naviga-tional challenge, which he defined ‘type III’, in which the birdwas able to return to a goal after being displaced (even artifi-cially) to an unknown area. Subsequently, the term ‘true navi-gation’ was adopted by Keeton (1974) to describe this,although Keeton used it as a term to describe all forms oforientation and navigation from unfamiliar area that were notexplained by other processes. This was problematic as truenavigation was defined by that which could not be explainedby other means, rather than as a testable hypothesis

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(Wiltschko & Wiltschko, 2003). However, over time, a work-able hypothesis for true navigation emerged as a number ofconsistent definitions and acknowledged true navigation to bethe ability to return to a known goal using only cues detectedlocally, not by cues detected during the displacement, forexample (Papi, 1992; Phillips, 1996; Able, 2001; Phillips,Schmidt-Koenig & Muheim, 2006). The most current defini-tion of true navigation is ‘the ability of an animal to return toits original location after displacement to a site in unfamiliarterritory, without access to familiar landmarks, goal emanat-ing cues, or information about the displacement route’(Phillips et al., 2006). This definition does not specifically rec-ognize migratory navigation, however, in which the displacedanimal may not be navigating to its original location prior todisplacement (i.e. homing) but a final breeding or winteringarea that it did not set out from. Hereafter, this is defined asmigratory true navigation: the ability of an animal to navigateto a specific breeding or wintering area (that it has not just setout from) following displacement.

Evidence for migratory true navigation

Initially, a series of displacement experiments on migratingbirds using mark/recapture techniques gathered evidence fortrue navigation (reviewed in Thorup & Holland, 2009). Theclearest example (Perdeck, 1958) demonstrated that adult butnot juvenile birds are capable of migratory true navigation.More recent studies have shown that adult, but not juvenilewhite-crowned sparrows are able to head towards their winterarea within the first 100 km of departure from the site ofdisplacement of 3700 km from their normal route duringautumn migration (Thorup et al., 2007), and that reed war-blers can correct for displacements of 1000 km during theirfirst return migration to their previous natal area (Chernetsov,Kishkinev & Mouritsen, 2008). Migratory true navigation isthus experience based, that is an ability to correct and returnto a known goal from an unfamiliar place is a consequence ofinformation learned on a previous journey to, or from thatgoal (Fig. 1). The test of true navigation is thus being able tocorrect after displacement to a novel location. A few studiessuggest that juvenile birds may in some circumstances appearto make corrections for displacements (Thorup & Rabøl,2001, 2007; Åkesson et al., 2005; Thorup et al., 2011), but it isnot clear whether this is the result of homing to a known goalalong the migratory route (e.g. the last known stopover site orthe natal area) or part of an inherited programme that allowsthem to compensate for displacements. Such a mechanism hasbeen described in sea turtles (Putman et al., 2011), but itremains to be seen whether either of these mechanisms exist,or the more common viewpoint of an inherited compass direc-tion is the only mechanism juveniles possess.

What is less often cited are the failures of displaced birds tocorrect for a displacement. For instance, a repeat of Perdeck’sstudy in which adult birds were displaced to Spain did notindicate that the birds could correct their orientation andreturn to the species winter area (Perdeck, 1967). White andgolden crowned sparrows Zonotrichia leucophrys gambelii andZ. altricapila, respectively, that were translocated from the US

to Korea from their winter grounds did not appear to returnto the US (Mewaldt, Cowley & Won, 1973). The fact thatsome birds make vast migrations that are global in nature isoften used to argue that true navigation ability must also beglobal (Bingman & Cheng, 2006), but these studies suggestthat there may be limits to the extent of a migratory truenavigation ability at least in the animals studied. Whethermigratory true navigation ability varies with migration dis-tance, or has a general limit in all birds is not yet known, butcurrent evidence does suggest variation, with the results ofThorup et al. (2007) indicating at least a 3700-km range, whileit appears shorter in starlings, possibly in the region of2000 km (Perdeck, 1967).

The theory of migratory true navigation

As the previous paragraph demonstrates, displacementexperiments provide evidence for true navigation ability, butnot for how they achieve it. Although not developed todescribe migratory true navigation specifically, the ‘map and

Breeding area

Winter area

Migratory corridor

A1

A2

B

Figure 1 Migratory true navigation (A1, A2) is distinct from homing (B)in that the goal is dependent upon the season. If displaced during thebreeding season, the animal homes to the same location. If displacedfrom the breeding ground during or just prior to migration, the animalwill navigate to the winter ground (A1), or if displaced from the winterground, to the breeding ground (A2). Whether this requires differentmechanisms or cues that homing has not yet been established.

Bird navigation R. A. Holland

2 Journal of Zoology •• (2014) ••–•• © 2014 The Zoological Society of London

compass’ hypothesis was developed by Kramer to explainnavigation behaviour by a process that comprises two 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 remainedthe most robust explanation for animal true navigation sinceits inception, and no significant challenge to the idea thatanimal navigation is a two-step process has been made. Truenavigation ability refers specifically to the ‘map’ step, theability to locate position with respect to a goal. Experiencedbirds are presumed to possess a ‘navigational map’, whichallows them to locate their position with respect to a final goaland navigate towards it using their compass sense. One theoryproposed that the map might work in a way akin to ourCartesian coordinate system, with animals able to refer toenvironmental gradients that vary predictably with latitudeand longitude (Fig. 2). For these gradients to be usable, theanimal would have to learn that they vary predictably in inten-sity with space (and possibly time) within their home rangeand extrapolate this beyond the learned area (Wallraff, 1974,1991). Thus, when displaced to an unfamiliar area the animalcould recognize a value in the gradients that was, for example,higher than the home range and recognize its displacementrelative to it. For a migratory bird, the presumption is that this

process of learning these values occurs before departing on thefirst migration for the breeding area, and during the firstwinter for the winter area. Thus, migratory birds are presumedto learn the value of gradients at two goals. This gradient maptends to be thought of as a two-cue system, often presumingthat a different environmental cue provides the longitude andlatitude equivalents. However, it has occasionally been sug-gested that different aspects of the same environmental cuecould form those two gradients [e.g. sun’s arc and sunrise time(Matthews, 1953), intensity and slope or inclination of themagnetic field (Walker, 1998; Boström, Åkesson & Alerstam,2012) ]. Thus, we know that migratory birds can perform truenavigation, and we have a theoretical construct for how theycould achieve this, but how do we study the nature of theenvironmental cues and sensory systems required to achievetrue navigation?

Studying migratory true navigation

The study of true navigation requires either displacement ofthe animal outside its familiar area, or a simulated displace-ment where an environmental cue is manipulated to representa different location than the one currently experienced. Theformer requires the ability to study the response to the dis-placement in the field, and the latter requires that the animalshows behaviour in the laboratory that correlates with orien-tation decisions in the wild. First, a laboratory-based correlateof migratory orientation exists in the form of migratory rest-lessness (Emlen & Emlen, 1966). This has been used with greatsuccess to investigate the nature of the magnetic compasssense in migrants (Wiltschko & Wiltschko, 1972; Wiltschkoet al., 1993; Ritz et al., 2004; Zapka et al., 2009). Orientationcages provide the potential for greater control as they can beperformed indoors. Surprisingly, orientation cage studies havenot been used as extensively to investigate the cues used in thenavigational map as they have the compass, despite the factthat testing orientation after displacement has been shown tobe possible (Thorup & Rabøl, 2007; Chernetsov et al., 2008)as are simulated displacement experiments (Fransson et al.,2001; Henshaw et al., 2010; Deutchlander, Phillips & Munro,2012). Second, recently, there have been calls for a returnto field-based study of true navigation in migratory birds(Wikelski et al., 2007; Thorup et al., 2010; Guilford et al.,2011). This stems from concerns that migratory restlessnessdoes not fully represent the behaviour of animals in the wild(Wikelski et al., 2007), and that we do not understand the fullextent of the challenges that animals face during migration(Holland et al., 2007). Animal movements in the wild can nowbe tracked using remote monitoring devices, which providethe precision that was lacking in mark recapture techniques.In some cases global positioning system (GPS) precisionis available and remote download from a satellite can beachieved [see Bridge et al. (2011) for a review of thetechnology currently available for tracking migratory birds].However, tracking devices that can follow a migratoryjourney with sufficient precision to test navigational decisionsare still too large for the small songbirds that remain the focusof much of true navigation in migration. As tracking of

Breeding

area

Winter area

4,5

–2,–3

–2 –3 –4 –5

–6

–5

–4

–3

–2

–1

Figure 2 In a bi-coordinate map, two gradients (represented by thebroad intersecting arrows A and B) are learned by exploration in thehome breeding area. As long as the gradients continue to increase ordecrease predictably, then if a bird is displaced, it can compare thevalues at the displaced location with those at the desired goal tocalculate the direction of displacement. Only by learning the values ofthe winter area can the bird navigate to it, and so migratory truenavigation can only be achieved by adult birds that have made a previ-ous journey.

R. A. Holland Bird navigation


migratory birds becomes more widespread, our understandingof the navigational challenges faced by both adults andjuveniles will increase, which will undoubtedly aid in adaptingthe theories of true navigation (Guilford et al., 2011).However, field-based studies of wild birds face the same inher-ent weaknesses as field-based studies in the other modelsystems, in that control of access to cues is difficult. Field-based studies of migration face the added difficulty of predict-ing both the timing of departure and goal of the animals. Theformer may cause problems in predicting the effect of treat-ments of sensory systems particularly when they are transi-tory, and the latter may increase the scatter in experimentalgroups, meaning an increase in the number of animals needed.Given that tracking technology remains relatively expensiveand studies are often restricted by the number of devices avail-able, this may lead to inconsistencies in results through lack ofstatistical power. Such studies are thus relatively rare, with nostudy of migratory true navigation using GPS telemetryhaving yet been published. The field thus relies on two imper-fect systems: a laboratory correlate that provides precisionand control, but which has limits in its relevance to naturalbehaviour, and a field-based system that is logistically difficultand lacks sufficient power at present.

The role of environmental cues intrue navigation

The sensory basis of the true navigation map contributes sig-nificantly to bird navigation’s reputation as a controversialfield. Many general reviews of migration that include achapter on navigation avoid discussion of this subtopic alto-gether (e.g. Dingle, 1996; Newton, 2007). Repeatability con-tinues to dog the field and certainly, interpreting findingswhere no effect of a treatment is obtained is problematic.However, simply ignoring the large amount of research thathas attempted to elucidate the sensory basis of true navigationdoes a disservice to the field. Without an understanding ofresearch that has attempted to understand this, advancescannot be made. The remainder of this review will thus assessthe experimental evidence for sensory cues in migratory birdnavigation, in the hope that understanding what has beentried, what has failed and what is incomplete will aid inmoving towards a resolution for this field.

Celestial cues

It has been proposed that animals could use celestial cues fornavigation (Matthews, 1951, 1953; Pennycuick, 1960). Boththe sun and stars can provide a cue to north-south positionbecause the zenith varies with latitude. Longitudinal displace-ment could potentially be detected if they were able to recog-nize that sun or star rise time was different from that at thegoal site. What is more, these provide a global reference frameand so in theory the animal’s position could be located any-where on the Earth so long as a view of the cue was available.However, both sun and star navigation are generally rejectedbased on two factors. First, tests on homing pigeons have

demonstrated that they have a time compensated sun com-pass that can be manipulated by shifting their internalclock (Schmidt-Koenig, 1960; Schmidt-Koenig, Ganzhorn &Ranvaud, 1991). This rejects sun navigation on two counts.First, it suggests that the birds (or at least homing pigeons) donot note the altitude of the sun, or they would not be fooled bythe shifts in their internal clock and thus do not use it as a cueto latitude. Second, a 6-h forward shift in the internal clockleads to a deflection of approximately 90° counter clockwise(i.e. to the west), matching the rate of movement of the sunacross the sky. This is not consistent with the use of the sun asa cue to longitude, which would be perceived as a displace-ment of approximately 5000 km to the west (i.e. the birdwould need to fly east to return home). It has been argued thatsuch displacements are unrealistic to a homing pigeon, and soa 6-h shift is an unrealistic test of the sun navigation hypoth-esis (Pennycuick, 1961). However, subsequent tests involvingmuch smaller shifts were also consistent with sun compass butnot sun navigation (Walcott & Michener, 1971). On this basis,sun navigation has been rejected (Baker, 1984). Clock shift hasalso been demonstrated in migratory birds in orientationcages, which might suggest it should be rejected for migratorytrue navigation (Able & Dillon, 1977; Able & Cherry, 1986;Muheim & Akesson, 2002), and one study did not support asignificant role for either the sun compass or sun navigation ina migrant songbird (Munro & Wiltschko, 1993).

The original experiments of Emlen, which established starsas a compass cue, actually provided some suggestion of timecompensation, although only with three birds (Emlen, 1967).However, subsequent investigation provided no evidence oftime compensation (Mouritsen & Larsen, 2001), withoutwhich longitude is not discernible. Additionally, there is noevidence for a clock mechanism playing a role in detectingdisplacements per se, which would preclude both star andsun navigation as a mechanism for longitude (Kishkinev,Chernetsov & Mouritsen, 2010). However, a meta-analysis ofdisplacement experiments of juvenile migratory birds in ori-entation cages suggests that they are more likely to correctunder starry skies than overcast skies, suggesting a role forcelestial cues in this behaviour (Thorup & Rabøl, 2007).Indeed, many studies of the role of sun and stars in migratorynavigation test only juvenile birds (e.g. Mouritsen & Larsen,2001, Muheim & Akesson, 2002), or the age is not reported(e.g. Able & Dillon, 1977, Able & Cherry, 1986). Rejection ofcelestial navigation thus relies to some extent on the assump-tion that the cues used by homing pigeons and migratory birdsare the same. It is however difficult to reconcile the globalavailability of celestial navigation with the apparent limits ontrue navigation in some migrating songbirds (see earlier).

Infrasound

Sounds in the range of 0.1–10 Hz are known to spread overhundreds if not thousands of miles. If stable, these have thepotential to act as a gradient for navigation. Evidence hasbeen presented that pigeon homing performance is disruptedby infrasound disturbance, such as disturbance of pigeonraces by sonic booms of aircraft (Hagstrum, 2000, 2001), or



fluctuations in orientation performance that correlate withatmospheric fluctuations (Hagstrum, 2013). The data, while inmany cases compelling, are correlational, however, making itdifficult to currently assess whether this is a result of disrup-tion of infrasound navigation cues, co-correlation with otherfactors propagated by atmospheric means, or disturbance inmotivation to home. An experiment, which removed thecochlea of homing pigeons did not produce any deficits inhoming performance (Wallraff, 1972), which, although notprecluding 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 navigationalmap question in pigeons. No experiment has yet demonstratedany effects of infrasound on bird migration. Nevertheless, itremains a viable cue which should be investigated further andthe range over which it could operate makes it a possibility forthe distances seen in migratory displacements.

Olfactory cues

No aspect of bird navigation contributes to its reputation as acontroversial field more than that of the role of olfactory cuesin the true navigation map. By far the majority of work hasinvolved 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 experi-ments is available in Wallraff (2005), and a detailed treatmentof all of these is beyond the scope of this review given that thefocus is on navigation in migratory birds,. However, olfactorynavigation is the most extensively tested hypothesis in truenavigation and as such its potential role in true navigation ofmigrants should be considered.

Key findings in olfactory navigation

Olfactory deprivation removes the ability of homing pigeonsto return to the home loft, and this is most clearly demon-strated by sectioning the olfactory nerve (Benvenuti et al.,1973; Gagliardo et al., 2006, 2008, 2009). Further key findingsin which orientation is altered rather than impaired have beenargued to suggest that the olfactory cues provide navigationalinformation to homing pigeons. A ‘false release site’ experi-ments in which birds were transported to a releases site in onedirection, allowed to sample air from this site, and then trans-ported to a release site in the opposite direction withoutfurther access to environmental odours found that birds flewin the direction expected if they were trying to home from theoriginal release site (Benvenuti & Wallraff, 1985). An experi-ment in which artificial odours (benzaldehyde) were presentedto pigeons at the loft from the north-west by fans found thatwhen displaced with benzaldehyde on their beaks, the birdsoriented in the direction consistent with a north-west displace-ment, rather than with the actual home direction (Ioale,Nozzolini & Papi, 1990). Further experiments in which loftsare shielded or winds are manipulated argued that pigeonslearn to associate odours brought by different wind directionswith different directions (Baldaccini et al., 1975; Ioale et al.,1978; Foa, Bagnoli & Giongo, 1986; Gagliardo et al., 2001).

In theory this does not require sampling of gradients as sug-gested by the bi-coordinate map, but merely associationbetween an odour and a direction.

Criticisms of olfactory navigation

Olfactory navigation has been criticized on a number ofcounts. First, lack of repeatability of the effects of olfactorydeprivation argues that olfaction is neither the only, nor anessential cue (Wiltschko, 1996). However, it is not clearwhether this lack of repeatability comes from redundancy innavigation cues or from variations caused by difficulties incontrol of the field-based system of experimentation, or in theexperiments themselves. If homing performance of birdstreated with zinc sulphate is considered, olfactory deprivationhas been demonstrated in a number of countries and on fourcontinents (Wallraff, 2005). A number of the key findings havealso been challenged. The deflector loft effect is shown in somecases to be a consequence of deflection of polarized light,involved in compass calibration, as anosmic birds still deflectafter exposure (Phillips & Waldvogel, 1982; Waldvogel,Phillips & Brown, 1988; Waldvogel & Phillips, 1991).However, the similar findings of experiments in which windsare reversed or shielded are not challenged by this discovery.The question of whether olfactory inputs are navigational orrelated to motivational factors has always been a concern ininterpretation (Wiltschko, 1996). In support of this, odoursappear to ‘activate’ other navigational processes in youngpigeons navigating by route reversal (Jorge, Marques &Phillips, 2009). Jorge et al. found that young pigeons, whichnavigate by route reversal, were unable to orient homeward iftransported in filtered air, but could if transported either withaccess to natural odours, or artificial ‘novel’ odours. Thisargues that smelling ‘non-home’ odours triggers the bird toaccess a navigation system based on other cues. The site simu-lation experiments of Benvenuti & Wallraff (1985) have alsobeen argued to be a consequence of activation of a naviga-tional map by non-navigational olfactory cues rather thannavigational in themselves (Jorge, Marques & Phillips, 2010).Presenting non-specific odours at the false release site pro-duced the same behaviour as access to natural odours. Asubsequent test of the activation hypothesis did not support arole for activation, however. Birds transported to a release sitewith access to novel odours were no more likely to orienthomewards than those transported in filtered air (Gagliardoet al., 2011). However, they used higher concentrations ofnovel odours than those used in the previous navigationexperiments, which it has been argued would make thepigeons anosmic (J.B Phillips, pers. Comm..). Nevertheless,the experiments of (Ioale et al., 1990) cannot be explained byactivation, as if the benzaldehyde odour was activating a non-olfactory navigational map, it would result in homeward ori-entation, not orientation consistent with a north-westdisplacement. One striking finding of the experiments onolfactory navigation in pigeons is that if olfactory navigationis correct, generally, it suggests that the view of redundancy ofcues is not correct. Where olfactory deprevation effects havebeen demonstrated they lead to significant impairment of



homing performance of pigeons at unfamiliar release sites,that is the majority do not return to the home loft. If olfactorycues are navigational, this argues that in their absence, no cuesare available to take their place, which goes against the widelyheld view that the navigational map must be made up ofredundant cues (Walcott, 1996; Wiltschko et al., 2010). Olfac-tory navigation thus continues to provide debate and perhapsfor this reason has not been widely accepted as an explanationfor true navigation in homing pigeons.

While the olfactory navigation hypothesis is by far the mostextensively tested when considering pigeon homing, it hasrarely been considered when discussing true navigation inmigrating birds. Stable odour gradients such as would be nec-essary for a bi-coordinate map have not been demonstrated toexist beyond approximately 200 km (Wallraff & Andreae,2000). This makes it difficult to explain the majority of dis-placement experiments on migrants by the use of olfactorynavigation. Nevertheless, two experiments on homing ofmigratory birds in the breeding season found a deficit in per-formance after olfactory deprivation (Fiaschi, Farina & Ioalé,1974; Wallraff et al., 1995). More surprisingly, a recent experi-ment demonstrated that adult catbirds displaced 1000 km eastfrom Illinois to Princeton in the US, subjected to olfactorydeprivation by zinc sulphate treatment and then radio-trackedfrom a light aircraft were unable to correct for the displace-ment in the way that controls were (Holland et al., 2009). Ifthis finding is borne out by further experimental support andshown to be a deficit based on the removal of navigation cues,then it may require a re-analysis of the bi-coordinate maptheory for true navigation. It appears to be hard to explainhow stable olfactory gradients could exist over the 1000 kmnecessary to explain this behaviour navigationally. Homingpigeons have not been shown to use olfactory cues beyond700 km, and then only if they had access to environmental airduring the displacement (Wallraff, 1981).

With regard to the use of olfactory signals by migrants, aninteresting parallel finding from a neurobiological study ofmigratory restlessness is that both visual and olfactory areasof the brain become more active at night during the migratoryperiod, while they are most active during the day outside thistime (Rastogi et al., 2011). This suggests that olfaction plays asignificant role in migratory behaviour, but it is still an openquestion as to what role this is. A recent hypothesis proposesthat in fact the primary role of olfaction across organisms (andthus reason for its evolution) is navigation (Jacobs, 2012). If itdoes indeed turn out to be the case, then theories of truenavigation based on a bi-coordinate map made stable envi-ronmental gradients may need to be significantly reconsid-ered, because olfactory cues do not seem to fit easily into thisparadigm.

Magnetic cues

The intensity of the Earth’s magnetic field was proposed as acue for bird navigation over a century ago (Viguier, 1882). TheEarth’s magnetic field is stronger at the poles than at theequator and it therefore has the potential to indicate latitudi-nal position. However, this is only functional over a relatively

coarse scale (Bingman & Cheng, 2006).There are variations inthe strength of the magnetic field at a fine scale, which meansit may be stronger at lower latitudes in some cases and varieswith longitude rather than latitude in other places (Phillipset al., 2006). Thus, even at a coarse scale, the magnetic fieldmay not be as consistent a cue to latitudinal position as it isoften portrayed. In seeming support of this, a number ofexperiments in which magnets are attached to the heads ofbirds homing over a long distance failed to find any deficit inhoming performance (Benhamou, Bonadonna & Jouventin,2003; Mouritsen et al., 2003; Bonadonna et al., 2005).However, since the 1960s, evidence of behavioural responsesto artificially changing the Earth’s magnetic field have beenobtained (Merkel & Wiltschko, 1965; Wiltschko & Wiltschko,1972). To date, at least 24 species of birds have been shown torespond to changes in the Earth’s magnetic field (Wiltschko &Wiltchko, 2007), but by far, the majority of studies onmagnetoreception in birds involve investigating its use as acompass, and it has been challenging to demonstrate the use ofthe magnetic field for a map (Phillips et al., 2006). Artificialdisplacement experiments, where the magnetic field is changedto indicate different latitudes to birds orienting in emlenfunnels, provide some support that birds recognize magneticintensity signatures as a cue to end migration (Fischer, Munro& Phillips, 2003; Henshaw et al., 2010). However, in thesestudies (performed on silvereyes Zosterops l. lateralis andlesser whitethroats Sylvia curruca) intensity signatures indicat-ing displacements outside of the normal range and migrationroute of the population did not produce navigationalresponses, as would be expected for a map cue. Instead theybecome disoriented. This may be a similar response to thatseen in juvenile migrants, in which magnetic ‘sign posts’ indi-cate latitudes at which innate compass directions must changefor successful migration (Beck & Wiltschko, 1988), and thusthe birds may merely stop migrating when a certain latitude isreached. Interestingly, this is also consistent with activation,as proposed for olfactory cues, with magnetic field signaturesactivating a non-magnetic navigation system below somethreshold value, but once that value is reached, the navigationsystem is no longer activated, even if the magnetic value is fargreater than the threshold. A recent follow-up study has indi-cated that only adults are affected by such magnetic displace-ments suggesting that it is a different behaviour than theinnate sign post recognition seen in juveniles (Deutchlanderet al., 2012). However, the lack of orientation towards thewinter site when the artificial displacement was north of itremained, making it difficult to conclude that the behaviourrepresented true navigation in the strict sense rather than anage-dependant response to latitudinal sign posts or activationof other navigational cues. Recall, however, that when(Perdeck, 1958) displaced adult starlings outside the winteringlatitude, they were able to correct and return to the normalwinter area. This indicates the challenge of orientation experi-ments: it is possible that different site fidelity is present in thedifferent species tested, with starlings showing more fidelity totheir winter site than silvereyes or lesser whitethroats, and thusthese 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 theirorientation in response to artificial displacements either northor south of their current position (Lohmann et al., 1995, 2004;Fischer et al., 2001). Experiments on the orientation perfor-mance of homing pigeons has also been shown to be disruptedat magnetic anomalies (areas with stronger or weaker mag-netic intensity than expected), which suggests that magneticintensity plays a role in their navigational map (Walcott, 1991;Dennis, Rayner & Walker, 2007; Mora & Walker, 2009;Wiltschko et al., 2010), although many of these experimentsare conducted within a range where the variation in magneticintensity is thought to make the earth’s magnetic field unreli-able as a cue to position (Phillips et al., 2006). This may indi-cate a different mechanism than that proposed for truenavigation in migrating birds, or perhaps that magnetic inten-sity correlates with other factors, which disrupt orientation inthese experiments (Wallraff, 2005). Part of the challenge indemonstrating a role for magnetic intensity has been becausemost navigational experiments involve sensory manipulation,and the way in which birds sense the magnetic field is by farthe most uncertain aspect of navigation research. However,within the last 20 years, significant advances have been madein this area. This has involved the integration of theoreticalwork from physics, biochemistry, neurobiology and molecularbiology alongside traditional behavioural experiments. As aconsequence, we now have an understanding of the way birdsmay perceive aspects of the magnetic field and how this maycontribute to the map and the compass aspects of true navi-gation. An understanding of the potential sensory pathways isthus crucial to understanding the behavioural experimentsthat support the use of the magnetic field as a map.

The magnetic sense: different receptors fordifferent tasks?

The behavioural evidence for magnetoreception was met withinitial scepticism because of the lack of an obvious senseorgan. However, consideration of physical principles of themagnetic field means that such sense organs need not belocated at the surface in the same way as photo or auditoryreceptors must: the Earth’s magnetic field can pervade alltissue. During the 1980s several models were proposed formagnetoreception, but two have withstood scrutiny: a mecha-nism based on photoreceptive molecules (the radical pairmechanism) and a mechanism based on magnetic iron parti-cles (the ferrimagnetic mechanism).

Radical pairs

Magnetically sensitive reactions involve radicals in whichunpaired electrons are present in different ‘spin’ states, eitherantiparallel (‘singlet’ state) or parallel (‘triplet’ state) (Rogers& Hore, 2009). The yield of the different states has been dem-onstrated to be influenced by strong magnetic fields, andbased on this, it was hypothesized that a molecule that formedsuch radicals in different yields depending on the magneticfield alignment could be the basis of a magnetoreceptor

(Schulten, Swenberg & Weller, 1978) (Fig. 3). It was subse-quently discovered that magnetic compass orientation isdependent on the wavelength of light (Wiltschko et al., 1993;Wiltschko & Wiltschko, 2006) and so the model was modifiedto suggest that the molecule involved in the radical pairprocess was photoreceptive and that a photon of lightwould instigate this reaction (Ritz, Adem & Schulten, 2000).Evidence that the magnetic compass was lateralized via theright eye to the left brain hemisphere suggested that the mag-netic field was perceived through the eyes [Wiltschko et al.,2002b; although see Hein et al. (2011) for evidence of nolateralization]. A study involving ZENK, an immediate earlygene, which is expressed in neurones, indicated that an area ofthe brain called cluster-N, responsible for night vision, wasactive during migratory restlessness (Mouritsen et al., 2005).A subsequent study in which this area of the brain waslesioned indicated that migratory robins could no longer usetheir magnetic compass (Zapka et al., 2009). Thus, migratorysongbirds appear to possess a magnetoreceptor mediated bythe visual system, which is based on a photoreceptive mol-ecule. Evidence that this is due to a radical pair mechanismcomes from an experiment based on the prediction that theinteraction between a radical pair and the magnetic field couldbe disrupted by a weak electromagnetic field in the radiospectrum (1.315 MHz, the so called Larmor frequency). It wasindeed the case that migratory robins could no longer orient inan emlen funnel when such a field was applied (Ritz et al.,

Singlet radical pair Triplet radical pair

Photoreceptive molecule

Light

Applied magnetic field

Signalling state

Yield A Yield B

Figure 3 A simplified schematic of the radical pair reaction. A photore-ceptive molecule forms radical pairs in the presence of specific wave-lengths of light. An applied magnetic field alters the yield of conversionbetween 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 & Hore, 2009) ]. It has been hypothesized that thissignalling state may be expressed as patterns on the retina, thusallowing the bird to see the magnetic field, but this has not yet beenconfirmed (Ritz et al., 2000) .



2004). The molecule involved has been proposed to be acryptochrome (Ritz et al., 2000). This is a blue light receptorand appears to form long-lived radical pairs, which would benecessary for it to work as a magnetoreceptor (Liedvogelet al., 2007). Four different cryptochromes have been found inthe eyes of migratory birds, Cry 1a, (Moller et al., 2004;Mouritsen et al., 2004; Niessner et al., 2011), Cry 1b (Molleret al., 2004), Cry 2 (Mouritsen et al., 2004) and Cry 4(Mouritsen et al., 2004). In terms of Fig. 3, it is thought thatthe radical pair comprises a flavosemiquinone radical and aterminal residue of a conserved triad of tryptophan residues (aflavin–tryptophan radical pair) (Biskup et al., 2009; Maedaet al., 2012). Based on our understanding of how a similarreaction occurs in plants, the flavosemiquinone radical wouldappear to lead to the signalling state (Bouly et al., 2007). Nodirect evidence yet exists however, to demonstrate thatcryptochrome is the primary sensing molecule involved inmagnetoreception (Liedvogel & Mouritsen, 2010; Mouritsen& Hore, 2012). More detailed discussion of the issues aroundthe radical pair compass can be found in (Rogers & Hore,2009; Mouritsen & Hore, 2012). What is crucial to this reviewis, Does it have a role in the navigational map? All the experi-ments described earlier involved disrupting the magneticcompass, in no case was there an indication that the radicalpair pathway is involved in map navigation. It does notappear that this mechanism detects intensity, nor indeed thepolarity 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 couldnot be involved in the navigational map, but no experimenthas tested this hypothesis. This may be due to the fact that itcould be challenging to design an experiment that is able todisentangle the use of the radical pair sense for a compassfrom its use in a map.

The ferrimagnetic sense

Ferrimagnetic materials are those in which spontaneous mag-netization occurs because the magnetic moments of atoms areopposed but unequal. This is seen in iron oxides, including theoldest known magnetic substance, magnetite. Ferrimagneticmaterial exists in a number of crystalline ‘domains’, includingmulti, single and supaparamagnetic. Multi domain magnetitehas no magnetization, single domain has a permanent mag-netic moment whereas superparamagnetic magnetite has afluctuating magnetic moment, but it can be aligned to anexternal magnetic field (Kirschvink & Walker, 1985). Basedon the discovery that bacteria containing single-domain mag-netite passively align to the magnetic field (Blakemore, 1975),and that magnetite is a biogenic material that is widely presentin the tissue of a diverse array of organisms, it was proposedthat such material could form the basis of a magnetic sense inmulticellular organisms (Yorke, 1979; Kirschvink & Gould,1981). To test this, it was proposed that the physical propertiesof the ferrimagnetic material could be used to predict thepresence of magnetic material in sensory cells in the same wayas it had been done in bacteria (Kirschvink, 1982). Ifferrimagnetic material was involved in a sensory receptor that

detected the Earth’s magnetic field, then a brief strong mag-netic pulse that exceeded the coercivity (the magnetic forcerequired to reduce the magnetization of the substance to zero)would re-magnetize the substance in the opposite direction ifapplied antiparallel to the original magnetization (Fig. 4).For most biogenic magnetite, the strength required tore-magnetize would be 0.1T, 5000 times the strength of theEarth’s magnetic field (Kirschvink & Walker, 1985;Kirschvink et al., 1985). If single-domain magnetite waspresent it would be re-magnetized, and if used by sensory cells,in theory, would lead to a change in the information thereceptor gave. Subsequently, a significant number of experi-ments have treated birds, with a strong magnetic pulse andindeed found that their orientation is affected by such a pulse.Effects have been found both on migratory birds tested inemlen funnels (Wiltschko et al., 1994, 1998; Beason, Dussourd& Deutschlander, 1995; Wiltschko & Wiltschko, 1995), innaturally migrating birds (Holland, 2010) and in homingpigeons (Beason, Wiltschko & Wiltschko, 1997). In all thesecases, a magnetic pulse leads to a deflection in orientation.However, where the pulse was applied antiparallel to thedirection of magnetization, the expected reorientation in theopposite direction did not occur (Wiltschko et al., 2002a;Holland, 2010). This is not consistent with single-domainmagnetite that is free to rotate in the way a bacteria cellcan and does not fit with the popularized concept of aferrimagnetic sense consisting of tiny compass needles(Mouritsen, 2012). Nor is the fact that the pulse effect appearsto be temporary, with birds returning to normal orientationafter approximately 10 days (Wiltschko et al., 1998, 2007;Wiltschko & Wiltchko, 2007). This does not support the

N

0.1T pulse

Figure 4 Chains of single-domain magnetite align with a biasing mag-netic field in the direction of magnetization (indicated by the red end).Application of a strong magnetic pulse antiparallel to the direction ofmagnetization will re-magnetize in the opposite direction. If such chainsare present in sensory cells and were free to rotate they would givedifferent information about the magnetic field after such a treatment.However, in practice, the effect of pulse treatments on birds do notclearly indicate that such structures exist.



permanent re-magnetization of magnetic material. One pulseexperiment demonstrated that the deflecting effect of the pulsewas removed if the ophthalmic branch of the trigeminal nerve(which innervates the beak) was anaesthetized with lidocane, alocal anaesthetic (Beason & Semm, 1996). This suggested thatthe magnetic pulse effected receptors located in the beak areaand the trigeminal nerve was responsible for conveying theinput from these receptors to the brain.

Two subsequent studies have confirmed the finding that thetrigeminal nerve conveys magnetic information. Mora et al.(2004) conditioned homing pigeons to a magnetic intensityanomaly, and found that they could no longer discriminate ifthe trigeminal nerve was lesioned [although see Kirschvink,Winklhofer & Walker (2010) for possible weaknesses in theexperimental design and Kishkinev, Mouritsen & Mora (2012)for failure to repeat the conditioning paradigm]. This indi-cated that the trigeminal nerve was responsible for conveyinginformation on the magnetic field. Following this, a study ofZENK expression indicated activation of neurons in thetrigeminal brainstem only in migratory robins orienting in amagnetic field that had an intact trigeminal nerve (Heyerset al., 2010). However, homing pigeons that had their trigemi-nal nerve lesioned were not disrupted in their homing perfor-mance (Gagliardo et al., 2006, 2008, 2009). Until recently, thismade the study of Beason & Semm (1996) the only study todate to indicate a role for the trigeminal nerve in the process ofnavigation, but what aspect of navigation? Lesions of thetrigeminal nerve do not appear to affect magnetic compassorientation in juvenile robins (Zapka et al., 2009), and thepulse deflects the orientation of birds in emlen funnels,but does not affect the magnetic compass (Munro et al.,1997b; Wiltschko & Wiltschko, 2006; Wiltschko et al., 2006).However, a particular design of pulse experiment suggests apossible role for the ferrimagnetic receptor in bird navigation.Pulses only appear to effect the orientation of adult migratingbirds, not juveniles (Munro et al., 1997a,b; Holland & Helm,2013), which suggests that the ferrimagnetic sense is involvedin an experience-based mechanism possessed by adult but notjuvenile birds. Because adults have true navigation, this sug-gests the ferrimagnetic sense is involved in the true navigationmap. A recent study has also shown that migrating reed war-blers returning to their breeding grounds, are unable to correctfor a displacement of 1000 km eastwards if the trigeminalnerve is cut, unlike intact and sham operated birds, who areable to do so (Kishkinev et al., 2013). This finding, on migra-tory birds, is in contrast to the findings on homing pigeons,where no role for the trigeminal nerve in navigation issupported.

On this basis it is argued that migrating birds possess twomagnetoreceptive pathways: a radical pair mechanism in theeye, which is responsible for at least compass orientation, anda ferrimagnetic sense, which is implicated in the detection ofmagnetic intensity and is involved in the navigational map(Wiltschko & Wiltchko, 2007). However, caution is urged inaccepting this interpretation without question. Adult but notjuvenile migratory birds have been shown to respond tochanges in intensity (Deutchlander et al., 2012) and adult butnot juvenile migratory birds have been shown to be affected by

a strong magnetic pulse (Munro et al., 1997a; Holland &Helm, 2013), but there is no direct causal link between the two.Similarly, the trigeminal nerve has been shown to be involvedin detecting the magnetic field (Mora et al., 2004), the pulseeffect no longer persists when this is anaesthetized, and migra-tory birds with trigeminal nerve section can no longer correctfor displacement (Kishkinev et al., 2013), but there is no directlink between the pulse and magnetic intensity, or the trigemi-nal nerve and magnetic intensity. Evidence for a ferrimagneticsense that is responsible for detecting intensity as part of a truenavigational map is thus based on several indirect links. Wedo not know for certain that the pulse affects a receptor thatdetects intensity, only that it changes navigation behaviourand that the behaviour appears to be mediated by the trigemi-nal nerve. To be certain of that, we would need to know thenature and location of the magnetic receptor.

The ferrimagnetic receptor: magnetite ormacrophage?

Initially, iron-containing cells found in the upper beak ofthe homing pigeons and other birds were suggested asmagnetoreceptors innervated via the trigeminal nerve,although no clear sensory receptor was identified (Beason &Nichols, 1984; Williams & Wild, 2001). A structure that hasthe potential to be a magnetic receptor has been described inthe beak of homing pigeons (Fleissner et al., 2003), chickensGallus domesticus, garden warblers Sylvia borin and robinsErithacus rubecula (Falkenberg et al., 2010). The structureappears to consist of sensory dendrites in the upper beak,which contains iron-rich bullets and an iron-containingvesicle. It is argued that these are distributed in such a way asto provide magnetic field information in three axes and thusform elements of a magnetometer. Appearing to support theargument that this is a magnetoreceptor, the effect of a mag-netic pulse disappears when the upper beak is anaesthetizedwith local anaesthetic (Wiltschko et al., 2009). The disruptingeffect of a magnetic anomaly on homing pigeon orientationalso disappears when the beak is anaesthetized (Wiltschkoet al., 2010). Again, however, the link is indirect. It is notcertain that the anaesthetic is acting directly on themagnetoreceptor in these experiments, and the effects of localanaesthetics have been questioned (Mouritsen & Hore, 2012).A further significant cautionary note to the beak-basedmagnetoreceptor theory has recently emerged. A thoroughstudy made on homing pigeons (Treiber et al., 2012) stronglysuggested that the majority of cells identified as containingiron, if not all, both in the upper beak and other parts of thebody, such as the skin, respiratory epithelium and featherfolliculi are macrophages, cells responsible for engulfing wasteand pathogens in the body. Treiber et al. (2012) argue that thestructures described in previous work are thus not sensorycells at all. This raises the question of whether amagnetoreceptor exists in the beak. However, the work ofTreiber et al. (2012) should not be over interpreted. While theburden of proof is on those who argue that the beak is the siteof magnetoreception (Mouritsen, 2012), Treiber et al. (2012)do acknowledge that there may be magnetoreceptors in some



as yet unidentified location in the beak. Added to this, anumber of behavioural studies supporting magnetoreceptionin the beak have been identified (Wiltschko & Wiltschko,2013).

A second potential site of a magnetoreceptor has alsobeen identified, in the inner ear lagena of homing pigeons,using electrophysiology recordings (Wu & Dickman, 2011,2012). Recent evidence from electron microscopy has identi-fied iron-rich cells in the inner ear (Lauwers et al., 2013),although they do not fit all the properties of a magne-toreceptor. Furthermore, experiments on homing pigeonsdid not show any deficit in homing with the inner earremoved (Wallraff, 1972), so unlike the beak-based sense,behavioural evidence is lacking.

Future perspectives: chronic disease or rudehealth?

As noted at the start of this review, a recent review ofmagnetoreception suggested that aspects of this field sufferedfrom a chronic disease in its lack of repeatability of findings(Mouritsen & Hore, 2012). It could be argued that this appliesequally to all aspects of bird navigation, with many experi-ments failing to repeat others, or contradictory results withinand between different disciplines. Does this mean thatresearch on bird navigation is in ill health? The assertion byMouritsen and Hore that experiments must be carefully con-trolled and designed to avoid observer bias is an importantone. However, the recent work of Treiber et al. (2012) thatquestions the structure and location of magnetoreceptorscould actually be viewed as a strength and sign of health: of afield that welcomes new results that may force revisions ofcurrent models of understanding. While many aspects of navi-gation are unresolved, as this review indicates, that does notmean that there is no data. While the models for studyingnavigation are imperfect, closer links between laboratorywork and field work are being established, and the addition ofnew technology for studying animals in the wild will broad-ened our understanding of the behaviour of migrating birdsand the challenges they face (Guilford et al., 2011). The inte-gration of neurobiology, physics and molecular biology intothe discipline is now well established and has led to a numberof breakthroughs in our understanding of the magnetic senseas well as the role of the olfactory sense in navigation. Theintegration of these disciplines has led to testable predictionsabout the structure of sensory systems and potentially themechanisms of navigation. For the field to advance further,the link between these disciplines and behavioural biologyneeds 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 sensewill allow better predictions about the effect of magnetic pulsetreatments to understand how receptors are changed by thetreatment. Strengthening this integration of other disciplines,while maintaining the roots as a behavioural biology disci-pline, will ultimately lead to the solution of the ‘mystery’ ofbird navigation. I will finish this review by highlighting some

of the key issues that should be resolved in order for the fieldof true navigation in migratory birds to advance.

Key questions in migratory true navigation

(1) Is the true navigation map unimodal, that is one environ-mental cue provides all information on location, bimodal, thatis two separate environmental cues provide different aspectsof the location (e.g. latitude and longitude), or redundant, thatis do multiple cues provide the same information for differentaspects of the location. Solving this will help to understandsome of the inconsistencies and conflicting evidence in thefield, as it will establish whether failure to repeat is a conse-quence of experimental design rather than redundancy ofcues.(2) Are there one or two magnetic sensory systems with dif-ferent functions? Clearly establishing whether the magnetite-based system is responsible for detecting intensity wouldestablish that not just direction, but also other aspects of themagnetic field could be used and form part of the magneticmap.(3) Related to (2), can a magnetite-based sensory receptor belocated and described? Understanding the structure of themagnetoreceptor will help to provide testable predictions forhow it might control birds’ behaviour, particularly in light ofthe pulse experiments.(4) To what extent does migratory behaviour in the wildmirror behaviour in an orientation cage? The field of naviga-tion now involves multiple disciplines including those outsidebiology and requires a controlled laboratory-based systemthat allows predictions to be tested by isolating cues. Theorientation cage provides this. However, currently, we havelittle understanding of how small songbirds respond to dis-placements in the wild with current techniques being toocoarse (ringing, geolocators) or lacking in range (radio track-ing). Understanding how songbirds respond to displacementsin more detail will indicate the range of their navigationsystem and thus the extent to which environmental cues willprovide reliable information on their location.(5) Is ‘activation’ a significant phenomenon within true navi-gation? The results of some experiments on both olfactory andmagnetic cues are consistent with them activating other navi-gational cues, but this would appear to violate the principle ofOccam’s razor by adding another step to the navigationprocess; if activation plays a part in true navigation, then itmoves from a two-step process (what is my location, whatdirection to reach home?) to a three-step process (am I athome? If no, what is my location, what direction to reachhome?), and the two cues providing the most evidence fornavigation (olfactory and magnetic) become relegated tointermediate steps towards the actual navigational cues.

AcknowledgementsI thank John Phillips and two anonymous reviewers forhelpful comments on the paper. Aspects of this review alsocame as a result of enjoyable discussions with the NavigationSpecial Interest Group at the MIGRATE NSF funded



meeting in Konstanz, 2010 with Susanna Åkesson,Verner Bingman, Tim Guilford, Anna Gagliardo, HenrikMouritsen, Rachel Muheim, Rosie Wiltschko and WolfgangWiltschko.

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true navigation in birds: from quantum physics to global migration

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