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True navigation in birds: from quantum physics to global migration
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Richard A. Holland
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School of Biological Sciences, Queen’s University of Belfast, 97 Lisburn Road, BT9 7BL,
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UK.
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Short title: Bird navigation
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Abstract
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Birds are capable of true navigation, the ability to return to a known goal from place they have
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never visited before. This is demonstrated most spectacularly during the vast migratory journeys
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made by these animals year after year often between continents and occasionally global in
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nature. However, it remains one of the great unanswered questions in science, despite more than
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50 years of research in this field. Nevertheless, the study of true navigation in birds has made
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significant advances in the previous 20 years, in part thanks to the integration of many
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disciplines outside its root in behavioural biology, to address questions of neurobiology,
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molecular aspects and the physics of sensory systems and environmental cues involved in bird
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navigation, often involving quantum physics. However, true navigation remains a controversial
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field, with many conflicting and confusing results making interpretation difficult, particularly for
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those outside or new to the field. Unlike many general texts on migration, which avoid
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discussion of these issues, this review will present these conflicting findings and assess the state
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of the field of true navigation during bird migration.
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Keywords: Navigation, Migration, Orientation, Bird, Magnetoreception, Olfaction, Map
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Introduction
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The apparent ability of migratory birds to make journeys of thousands of miles, crossing deserts,
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oceans and mountain ranges, sometimes even circumnavigating the globe has long fascinated
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both scientists and laymen alike. Fifty years of intensive research on the mechanisms and
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sensory cues required have revealed much about the way birds can achieve this feat of navigation
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with such precision but also leaves many open questions and the field is one that is seen as beset
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with controversy over conflicting results (Alerstam, 2006). Recently, this problem was described
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as a “chronic disease” (Mouritsen and Hore, 2012), suggesting that the field is unhealthy, in a
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scientific sense, and data should not be trusted. The “mystery” of how birds navigate continues
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to be alluded to both in popular and professional media (Baker, 1984, HollandThorup and
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Wikelski, 2007), and remains one of the great unanswered questions in science (Kennedy and
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Norman, 2005) but in the last 20 years animal navigation has taken huge strides forwards by
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becoming a truly interdisciplinary field. Researchers from physical, chemical, histological,
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neuropysiological and electrophysiological disciplines all contribute to our understanding of bird
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navigation and a researcher working in this field must now cast their literature search far wider
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than the traditional behaviour focused journals that the early work was published in. This
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combination of a difficulty in interpreting conflicting results and the diverse fields which
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contribute to our understanding of bird navigation may make a daunting prospect for those new
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to the subject. It is thus the aim of this review to assess these conflicting results and integrate the
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new information from other disciplines from the perspective of a behavioural biologist working
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at the level of the organism, in order to make the field more accessible to new scientists entering
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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
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that must be tackled if the subject is to be resolved.
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Migratory true navigation
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What is true navigation?
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Donald Griffin was the first to conceptualise bird navigation (Griffin, 1952) and he recognised a
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specific form of navigational challenge, which he defined “type III”, in which the bird was able
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to return to a goal after being displaced (even artificially) to an unknown area. Subsequently the
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term “true navigation” was adopted to describe this by Keeton (Keeton, 1974), although Keeton
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used it as a term to describe all forms of orientation and navigation from unfamiliar area that
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were not explained by other processes. This was problematic as true navigation was defined by
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that which could not be explained by other means, rather than as a testable hypothesis (Wiltschko
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and Wiltschko, 2003). However, over time a workable hypothesis for true navigation emerged as
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a number of consistent definitions acknowledged true navigation to be the ability to return to a
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known goal using only cues detected locally, not by cues detected during the displacement e.g.
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(Able, 2001, Phillips, 1996, Papi, 1992, PhillipsSchmidt-Koenig and Muheim, 2006). The most
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current definition of true navigation is “the ability of an animal to return to its original location
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after displacement to a site in unfamiliar territory, without access to familiar landmarks, goal
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emanating cues, or information about the displacement route” (Phillips et al., 2006). This
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definition does not specifically recognise migratory navigation however, in which the displaced
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animal may not be navigating to its original location prior to displacement (i.e. homing) but a
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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
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it has not just set out from) following displacement.
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Evidence for migratory true navigation
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Initially, a series of displacement experiments on migrating birds using mark/recapture
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techniques gathered evidence for true navigation (reviewed in (Thorup and Holland, 2009)). The
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clearest example (Perdeck, 1958) demonstrated that adult but not juvenile birds are capable of
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migratory true navigation. More recent studies have shown that adult, but not juvenile white
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crowned sparrows are able to head towards their winter area within the first 100km of departure
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from the site of displacement of 3700km from their normal route during autumn migration
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(Thorup et al., 2007), and that reed warblers can correct for displacements of 1000km during
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their first return migrating to their previous natal area (ChernetsovKishkinev and Mouritsen,
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2008). Migratory true navigation is thus experience based, i.e. an ability to correct and return to a
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known goal from an unfamiliar place is a consequence of information learned on a previous
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journey to, or from that goal (figure 1). The test of true navigation is thus being able to correct
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after displacement to a novel location. A few studies suggest that juvenile birds may in some
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circumstances appear to make corrections for displacements (Thorup et al., 2011, Thorup and
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Rabøl, 2007, Thorup and Rabøl, 2001, Åkesson et al., 2005), but it is not clear whether this is the
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result of homing to a known goal along the migratory route (e.g. the last known stopover site or
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the natal area) or part of an inherited programme that allows them to compensate for
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displacements. Such a mechanism has been described in sea turtles (Putman et al., 2011), but it
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remains to be seen whether either of these mechanisms exist, or the more common viewpoint of
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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.
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For instance, a repeat of Perdeck’s study in which adult birds were displaced to Spain did not
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indicate that the birds could correct their orientation and return to the species winter area
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(Perdeck, 1967). White and Golden crowned sparrows (Zonotrichia leucophrys gambelii and Z.
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altricapila) that were translocated from the USA to Korea from their winter grounds did not
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appear to return to the USA (MewaldtCowley and Won, 1973). The fact that some birds make
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vast migrations that are global in nature is often used to argue that true navigation ability must
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also be global (Bingman and Cheng, 2006), but these studies suggest that there may be limits to
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the extent of a migratory true navigation ability at least in the animals studied. Whether
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migratory true navigation ability varies with migration distance, or has a general limit in all birds
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is not yet known, but current evidence does suggest variation, with the results of Thorup et al.
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(2007) indicating at least a 3700km range, while it appears shorter in Starlings, possibly in the
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region of 2000km (Perdeck, 1967).
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The theory of migratory true navigation.
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As the previous paragraph demonstrates, displacement experiments provide evidence for true
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navigation ability, but not for how they achieve it. Although not developed to describe migratory
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true navigation specifically, the “map and compass” hypothesis was developed by Kramer to
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explain navigation behaviour by a process that comprises 2 steps, determining position with
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respect to the goal, “the map step” and determining direction to a goal, “the compass step”
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(Kramer, 1953). The map and compass theory has remained the most robust explanation for
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animal true navigation since its inception and no significant challenge to the idea that animal
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navigation is a two-step process has been made. True navigation ability refers specifically to the
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“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
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goal and navigate towards it using their compass sense. One theory proposed that the map might
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work in a way akin to our Cartesian coordinate system, with animals able to refer to
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environmental gradients that vary predictably with latitude and longitude (figure 2). For these
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gradients to be usable, the animal would have to learn that they vary predictably in intensity with
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space (and possibly time) within their home range and extrapolate this beyond the learned area
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(Wallraff, 1991, Wallraff, 1974). Thus when displaced to an unfamiliar area the animal could
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recognise a value in the gradients that was, for example, higher than the home range and
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recognise its displacement relative to it. For a migratory bird, the presumption is that this process
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of learning these values occurs before departing on the first migration for the breeding area, and
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during the first winter for the winter area. Thus, migratory birds are presumed to learn the value
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of gradients at 2 goals. This gradient map tends to be thought of as a 2 cue system, often
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presuming that a different environmental cue provides the longitude and latitude equivalents.
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However, it has occasionally been suggested that different aspects of the same environmental cue
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could form those two gradients (e.g. sun’s arc and sunrise time (Matthews, 1953), intensity and
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slope or inclination of the magnetic field (Walker, 1998, BoströmÅkesson and Alerstam, 2012)).
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Thus, we know that migratory birds can perform true navigation, and we have a theoretical
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construct for how they could achieve this, but how do we study the nature of the environmental
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cues and sensory systems required to achieve true navigation?
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Studying migratory true navigation
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The study of true navigation requires either displacement of the animal outside its familiar area,
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or a simulated displacement where an environmental cue is manipulated to represent a different
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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
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laboratory that correlates with orientation decisions in the wild. First, a laboratory based
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correlate of migratory orientation exists in the form of migratory restlessness (Emlen and Emlen,
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1966). This has been used with great success to investigate the nature of the magnetic compass
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sense in migrants (Wiltschko and Wiltschko, 1972, Ritz et al., 2004, Wiltschko et al., 1993,
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Zapka et al., 2009). Orientation cages provide the potential for greater control as they can be
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performed indoors. Surprisingly, orientation cage studies have not been used as extensively to
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investigate the cues used in the navigational map as they have the compass, despite the fact that
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testing orientation after displacement has been shown to be possible (Thorup and Rabøl, 2007,
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Chernetsov et al., 2008) as are simulated displacement experiments (Fransson et al., 2001,
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Henshaw et al., 2010, DeutchlanderPhillips and Munro, 2012). Second, recently there have been
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calls for a return to field based study of true navigation in migratory birds (Guilford et al., 2011,
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Thorup et al., 2010, Wikelski et al., 2007). This stems from concerns that migratory restlessness
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does not fully represent the behaviour of animals in the wild (Wikelski et al., 2007), and that we
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do not understand the full extent of the challenges that animals face during migration (Holland et
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al., 2007). Animal movements in the wild can now be tracked using remote monitoring devices
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that provide the precision that was lacking in mark recapture techniques. In some cases GPS
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precision is available and remote download from a satellite can be achieved (see (Bridge et al.,
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2011) for review of currently available technology for tracking migratory birds). However,
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tracking devices that can follow a migratory journey with sufficient precision to test navigational
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decisions are still too large for the small songbirds that remain the focus of much of true
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navigation in migration. As tracking of migratory birds becomes more widespread, our
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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).
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However, field based study of wild birds faces the same inherent weaknesses as field based study
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in the other model systems, in that control of access to cues is difficult. Field based study of
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migration faces the added difficulty of predicting both the timing of departure and goal of the
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animals. The former may cause problems in predicting the effect of treatments of sensory
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systems particularly when they are transitory and the latter may increase the scatter in
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experimental groups, meaning an increase in the number of animals needed. Given that tracking
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technology remains relatively expensive and studies are often restricted by the number of devices
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available, this may lead to inconsistencies in results through lack of statistical power. Such
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studies are thus relatively rare, with no study of migratory true navigation using GPS telemetry
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having yet been published. The field thus relies on two imperfect systems, a laboratory correlate
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that provides precision and control, but which has limits in its relevance to natural behaviour,
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and a field based system that is logistically difficult and lacks sufficient power at present.
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The role of environmental cues in true navigation
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The sensory basis of the true navigation map contributes significantly to bird navigation’s
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reputation as a controversial field. Many general reviews of migration that include a chapter on
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navigation avoid discussion of this sub-topic altogether (e.g. (Newton, 2007, Dingle, 1996)).
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Repeatability continues to dog the field and certainly, interpreting findings where no effect of a
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treatment is obtained is problematic. However, simply ignoring the large amount of research that
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has attempted to elucidate the sensory basis of true navigation does a disservice to the field.
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Without an understanding of research that has attempted to understand this, advances cannot be
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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
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and what is incomplete will aid in moving towards a resolution for this field.
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Celestial cues
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It has been proposed that animals could use celestial cues for navigation (Matthews, 1953,
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Matthews, 1951, Pennycuick, 1960). Both the sun and stars can provide a cue to north-south
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position because the zenith varies with latitude. Longitudinal displacement could potentially be
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detected if they were able to recognise that sun or star rise time was different from that at the
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goal site. What is more, these provide a global reference frame and so in theory the animal’s
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position could be located anywhere on the Earth so long as a view of the cue was available.
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However, both sun and star navigation are generally rejected based on two factors. First, tests on
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homing pigeons have demonstrated that they have a time compensated sun compass that can be
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manipulated by shifting their internal clock (Schmidt-KoenigGanzhorn and Ranvaud, 1991,
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Schmidt-Koenig, 1960). This rejects sun navigation on two counts. First, it suggests that the
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birds (or at least homing pigeons) do not note the altitude of the sun, or they would not be fooled
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by the shifts in their internal clock and thus do not use it as a cue to latitude. Second, a 6 hour
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forward shift in the internal clock leads to a deflection of approximately 90° counter clockwise
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(i.e. to the west), matching the rate of movement of the sun across the sky. This is not consistent
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with the use of the sun as a cue to longitude, which would be perceived as a displacement of
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approximately 5000km to the west (i.e. the bird would need to fly east to return home). It has
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been argued that such displacements are unrealistic to a homing pigeon, and so a six hour shift is
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an unrealistic test of the sun navigation hypothesis (Pennycuick, 1961). However, subsequent
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tests involving much smaller shifts were also consistent with sun compass but not sun navigation
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(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
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suggest it should be rejected for migratory true navigation (Able and Cherry, 1986, Able and
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Dillon, 1977, Muheim and Akesson, 2002), and one study did not support a significant role for
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either the sun compass or sun navigation in a migrant songbird (Munro and Wiltschko, 1993).
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The original experiments of Emlen, which established stars as a compass cue , actually
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provided some suggestion of time compensation, although only with three birds (Emlen, 1967).
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However, subsequent investigation provided no evidence of time compensation (Mouritsen and
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Larsen, 2001), without which longitude is not discernible. Additionally, there is no evidence for
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a clock mechanism playing a role in detecting displacements per se, which would preclude both
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star and sun navigation as a mechanism for longitude (KishkinevChernetsov and Mouritsen,
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2010). However, a meta-analysis of displacement experiments of juvenile migratory birds in
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orientation cages suggests that they are more likely to correct under starry skies than overcast
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skies, suggesting a role for celestial cues in this behaviour (Thorup and Rabøl, 2007). Indeed,
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many studies of the role of sun and stars in migratory navigation test only juvenile birds (e.g.
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Mouritsen and Larsen 2001, Muheim and Akesson 2002), or the age is not reported (e.g. Able
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and Dillon 1977, Able and Cherry 1986). Rejection of celestial navigation thus relies to some
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extent on the assumption that the cues used by homing pigeons and migratory birds are the same.
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It is however difficult to reconcile the global availability of celestial navigation with the apparent
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limits on true navigation in some migrating songbirds (see above).
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Infrasound
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Sounds in the range of 0.1-10 Hz are known to spread over hundreds if not thousands of miles. If
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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
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pigeon races by sonic booms of aircraft (Hagstrum, 2000, Hagstrum, 2001), or fluctuations in
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orientation performance that correlate with atmospheric fluctuations (Hagstrum, 2013). The data,
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while in many cases compelling, are correlational however, making it difficult to currently assess
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whether this is a result of disruption of infrasound navigation cues, co-correlation with other
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factors propagated by atmospheric means, or disturbance in motivation to home. An experiment
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which removed the cochlea of homing pigeons did not produce any deficits in homing
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performance (Wallraff, 1972), which, although not precluding that infrasound is part of a
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multifactorial map, does not support the argument made by (Hagstrum, 2013) that infrasonic
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cues are the sole solution to the navigational map question in pigeons. No experiment has yet
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demonstrated any effects of infrasound on bird migration. Nevertheless, it remains a viable cue
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which should be investigated further and the range over which it could operate makes it a
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possibility for the distances seen in migratory displacements.
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Olfactory cues
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No aspect of bird navigation contributes to its reputation as a controversial field more than that
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of the role of olfactory cues in the true navigation map. By far the majority of work has involved
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homing pigeons and a large number of experiments, possibly more than in any other aspect of
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bird true navigation, have been performed. A comprehensive review of these experiments is
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available in (Wallraff, 2005) and a detailed treatment of all of these is beyond the scope of this
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review given that the focus is on navigation in migratory birds,. However, olfactory navigation is
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the most extensively tested hypothesis in true navigation and as such its potential role in true
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navigation of migrants should be considered.
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Key findings in olfactory navigation
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Olfactory deprivation removes the ability of homing pigeons to return to the home loft, and this
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is most clearly demonstrated by sectioning the olfactory nerve (Gagliardo et al., 2006, Gagliardo
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et al., 2008, Gagliardo et al., 2009, Benvenuti et al., 1973). Further key findings in which
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orientation is altered rather than impaired have been argued to suggest that the olfactory cues
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provide navigational information to homing pigeons. A ‘false release site’ experiments in which
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birds were transported to a releases site in one direction, allowed to sample air from this site, and
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then transported to a release site in the opposite direction without further access to environmental
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odours found that birds flew in the direction expected if they were trying to home from the
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original release site (Benvenuti and Wallraff, 1985). An experiment in which artificial odours
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(benzaldehyde) were presented to pigeons at the loft from the north west by fans found that when
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displaced with benzaldehyde on their beaks, the birds oriented in the direction consistent with a
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north west displacement, rather than with the actual home direction (IoaleNozzolini and Papi,
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1990). Further experiments in which lofts are shielded or winds are manipulated argued that
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pigeons learn to associate odours brought by different wind directions with different directions
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(Baldaccini et al., 1975, Ioale et al., 1978, FoaBagnoli and Giongo, 1986, Gagliardo et al., 2001).
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In theory this does not require sampling of gradients as suggested by the bi-coordinate map, but
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merely association between an odour and a direction.
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Criticisms of olfactory navigation
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Olfactory navigation has been criticised on a number of counts. First, lack of repeatability of the
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effects of olfactory deprivation argues that olfaction is neither the only, nor an essential cue
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(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
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based system of experimentation, or in the experiments themselves. If homing performance of
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birds treated with zinc sulphate is considered, olfactory deprivation has been demonstrated in a
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number of countries and on four continents (Wallraff, 2005). A number of the key findings have
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also been challenged. The deflector loft effect is shown in some cases to be a consequence of
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deflection of polarized light, involved in compass calibration, as anosmic birds still deflect after
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exposure (Phillips and Waldvogel, 1982, Waldvogel and Phillips, 1991, WaldvogelPhillips and
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Brown, 1988). However, the similar findings of experiments in which winds are reversed or
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shielded are not challenged by this discovery. The question of whether olfactory inputs are
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navigational or related to motivational factors has always been a concern in interpretation
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(Wiltschko, 1996). In support of this odours appear to ‘activate’ other navigational processes in
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young pigeons navigating by route reversal (JorgeMarques and Phillips, 2009). Jorge et al. found
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that young pigeons, which navigate by route reversal, were unable to orient homeward if
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transported in filtered air, but could if transported either with access to natural odours, or
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artificial ‘novel’ odours. This argues that smelling ‘non-home’ odours I, triggers the bird to
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access a navigation system based on other cues. The site simulation experiments of Benvenuti
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and Wallraff (1985) have also been argued to be a consequence of activation of a navigational
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map by non-navigational olfactory cues rather than navigational in themselves (JorgeMarques
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and Phillips, 2010). Presenting non-specific odours at the false release site produced the same
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behaviour as access to natural odours. A subsequent test of the activation hypothesis did not
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support a role for activation however, birds transported to a release site with access to novel
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odours were no more likely to orient homewards than those transported in filtered air (Gagliardo
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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
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(Phillips, personal communication). However, the experiments of (Ioale et al., 1990) cannot be
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explained by activation, as if the benzaldehyde odour was activating a non-olfactory navigational
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map, it would result in homeward orientation, not orientation consistent with a north west
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displacement. One striking finding of the experiments on olfactory navigation in pigeons is that
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if olfactory navigation is correct generally, it suggests that the view of redundancy of cues is not
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correct. Where olfactory deprevation effects have been demonstrated they lead to significant
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impairment of homing performance of pigeons at unfamiliar release sites, i.e. the majority do not
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return to the home loft. If olfactory cues are navigational, this argues that in their absence no
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cues are available to take their place which goes against the widely held view that the
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navigational map must be made up of redundant cues (Walcott, 1996, Wiltschko et al., 2010).
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Olfactory navigation thus continues to provide debate and has not been widely accepted as an
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explanation for true navigation in homing pigeons.
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While the olfactory navigation hypothesis is by far the most extensively tested when
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considering pigeon homing, it has rarely been considered when discussing true navigation in
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migrating birds. Stable odour gradients such as would be necessary for a bi-coordinate map have
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not been demonstrated to exist beyond approximately 200km (Wallraff and Andreae, 2000). This
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makes it difficult to explain the majority of displacement experiments on migrants by the use of
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olfactory navigation. Nevertheless, two experiments on homing of migratory birds in the
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breeding season found a deficit in performance after olfactory deprivation (Wallraff et al., 1995,
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FiaschiFarina and Ioalé, 1974). More surprisingly, a recent experiment demonstrated that adult
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catbirds displaced 1000km east from Illinois to Princeton in the USA, subjected to olfactory
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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
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borne out by further experimental support and shown to be a deficit based on removal of
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navigation cues, then it may require a re-analysis of the bi-coordinate map theory for true
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navigation. It appears to be hard to explain how stable olfactory gradients could exist over the
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1000km necessary to explain this behaviour navigationally. Homing pigeons have not been
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shown to use olfactory cues beyond 700km, and then only if they had access to environmental air
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during the displacement (Wallraff, 1981).
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With regard to the use of olfactory signals by migrants, an interesting parallel finding
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from a neurobiological study of migratory restlessness is that both visual and olfactory areas of
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the brain become more active at night during the migratory period, while they are most active
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during the day outside this time (Rastogi et al., 2011). This suggests that olfaction plays a
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significant role in migratory behaviour, but it is still an open question as to what role this is. A
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recent hypothesis proposes that in fact the primary role of olfaction across organisms (and thus
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reason for its evolution) is navigation (Jacobs, 2012). If it does indeed turn out to be the case
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then theories of true navigation based on a bi-coordinate map made stable environmental
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gradients may need to be significantly reconsidered, since olfactory cues do not seem to fit easily
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into this paradigm.
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Magnetic cues
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The intensity of the Earth’s magnetic field was proposed as a cue for bird navigation over a
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century ago (Viguier, 1882). The Earth’s magnetic field is stronger at the poles than at the
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equator and it therefore has the potential to indicate latitudinal position. However, this is only
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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
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some cases and varies with longitude rather than latitude in some places (Phillips et al., 2006).
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Thus, even at a coarse scale the magnetic field may not be as consistent a cue to latitudinal
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position as it is often portrayed. In seeming support of this, a number of experiments in which
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magnets are attached to the heads of birds homing over long distance failed to find any deficit in
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homing performance (BenhamouBonadonna and Jouventin, 2003, Bonadonna et al., 2005,
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Mouritsen et al., 2003). However, since the 1960’s evidence of behavioural responses to
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artificially changing the Earth’s magnetic field have been obtained (Merkel and Wiltschko, 1965,
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Wiltschko and Wiltschko, 1972). To date at least 24 species of bird have been shown to respond
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to changes in the Earth’s magnetic field (Wiltschko and Wiltchko, 2007) but by far the majority
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of studies on magnetoreception in birds involve investigating its use as a compass and it has been
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challenging to demonstrate the use of the magnetic field for a map (Phillips et al., 2006).
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Artificial displacement experiments, where the magnetic field is changed to indicate different
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latitudes to birds orienting in emlen funnels, provide some support that birds recognise magnetic
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intensity signatures as a cue to end migration (Henshaw et al., 2010, FischerMunro and Phillips,
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2003). However, in these studies (performed on Silvereyes, Zosterops l. lateralis and Lesser
351
Whitethroats Sylvia curruca) intensity signatures indicating displacements outside of the normal
352
range and migration route of the population did not produce navigational responses, as would be
353
expected for a map cue. Instead they become disoriented. This may be a similar response to that
354
seen in juvenile migrants, in which magnetic “sign posts” indicate latitudes at which innate
355
compass directions must change for successful migration (Beck and Wiltschko, 1988) and thus
356
the birds may merely stop migrating when a certain latitude is reached. Interestingly, this is also
357
consistent with activation, as proposed for olfactory cues, with magnetic field signatures
358
activating a non-magnetic navigation system below some threshold value, but once that value is
359
reached, the navigation system is no longer activated, even if the magnetic value is far greater
360
than the threshold. A recent follow-up study has indicated that only adults are affected by such
361
magnetic displacements suggesting that it is a different behaviour than the innate signpost
362
recognition seen in juveniles (Deutchlander et al., 2012). However, the lack of orientation
363
towards the winter site when the artificial displacement was north of it remained, making it
364
difficult to conclude that the behaviour represented true navigation in the strict sense rather than
365
an age dependant response to latitudinal sign posts, or activation of other navigational cues.
366
Recall however, that when (Perdeck, 1958) displaced adult starlings outside the wintering
367
latitude, they were able to correct and return to the normal winter area. This indicates the
368
challenge of orientation experiments: it is possible that different site fidelity is present in the
369
different species tested, with starlings showing more fidelity to their winter site than Silvereyes
370
or Lesser Whitethroats, and thus these two species do not represent the ideal model for this test.
371
Contrast this to similar experiments on newts, turtles and spiny lobsters, which have been
372
demonstrated to alter their orientation in response to artificial displacements either north or south
373
of their current position (Fischer et al., 2001, Lohmann et al., 2004, Lohmann et al., 1995).
374
Experiments on the orientation performance of homing pigeons has also been shown to be
375
disrupted at magnetic anomalies (areas with stronger or weaker magnetic intensity than
376
expected), which suggests that magnetic intensity plays a role in their navigational map
377
(DennisRayner and Walker, 2007, Walcott, 1991, Wiltschko et al., 2010, Mora and Walker,
378
2009), although many of these experiments are conducted within a range where the variation in
379
magnetic intensity is thought to make the earth’s magnetic field unreliable as a cue to position
380
(Phillips et al., 2006). This may indicate a different mechanism than that proposed for true
381
navigation in migrating birds, or perhaps that magnetic intensity correlates with other factors
382
which disrupt orientation in these experiments (Wallraff, 2005). Part of the challenge in
383
demonstrating a role for magnetic intensity has been because most navigational experiments
384
involve sensory manipulation, and the way in which birds sense the magnetic field is by far the
385
most uncertain aspect of navigation research. However, within the last 20 years, significant
386
advances have been made in this area. This has involved the integration of theoretical work from
387
physics, biochemistry, neurobiology and molecular biology alongside traditional behavioural
388
experiments. As a consequence, we now have an understanding of the way birds may perceive
389
aspects of the magnetic field and how this may contribute to the map and the compass aspects of
390
true navigation. An understanding of the potential sensory pathways is thus crucial to
391
understanding the behavioural experiments that support the use of the magnetic field as a map.
392
The magnetic sense: different receptors for different tasks?
393
The behavioural evidence for magnetoreception was met with initial scepticism due to the lack of
394
an obvious sense organ. However, consideration of physical principles of the magnetic field
395
means that such sense organs need not be located at the surface in the same way as photo or
396
auditory receptors must: the Earth’s magnetic field can pervade all tissue. During the 1980’s
397
several models were proposed for magnetoreception but 2 have withstood scrutiny: a mechanism
398
based on photoreceptive molecules (the radical pair mechanism) and a mechanism based on
399
magnetic iron particles (the ferrimagnetic mechanism).
400
Radical pairs
401
Magnetically sensitive reactions involve radicals in which unpaired electrons are present in
402
different “spin” states, either antiparallel (“singlet” state) or parallel (“triplet” state) (Rogers and
403
Hore, 2009). The yield of the different states has been demonstrated to be influenced by strong
404
magnetic fields, and based on this it was hypothesised that a molecule that formed such radicals
405
in different yields depending on the magnetic field alignment could be the basis of a
406
magnetoreceptor (SchultenSwenberg and Weller, 1978) (figure 3). It was subsequently
407
discovered that magnetic compass orientation is dependent on the wavelength of light (Wiltschko
408
et al., 1993, Wiltschko and Wiltschko, 2006) and so the model was modified to suggest that the
409
molecule involved in the radical pair process was photoreceptive and that a photon of light
410
would instigate this reaction (RitzAdem and Schulten, 2000). Evidence that the magnetic
411
compass was lateralized via the right eye to the left brain hemisphere suggested that the magnetic
412
field was perceived through the eyes (Wiltschko et al., 2002b), although see (Hein et al., 2011)
413
for evidence of no lateralization. A study involving ZENK, an immediate early gene which is
414
expressed in neurones indicated that an area of the brain called cluster-N, responsible for night
415
vision was active during migratory restlessness (Mouritsen et al., 2005). A subsequent study in
416
which this area of the brain was lesioned indicated that migratory robins could no longer use
417
their magnetic compass (Zapka et al., 2009). Thus, migratory songbirds appear to possess a
418
magnetoreceptor mediated by the visual system which is based on a photoreceptive molecule.
419
Evidence that this is because of a radical pair mechanism comes from an experiment based on
420
the prediction that the interaction between a radical pair and the magnetic field could be
421
disrupted by a weak electromagnetic field in the radio spectrum (1.315 MHz, the so called
422
Larmor frequency). It was indeed the case that migratory robins could no longer orient in an
423
emlen funnel when such a field was applied (Ritz et al., 2004). The molecule involved has been
424
proposed to be a cryptochrome (Ritz et al., 2000). This is a blue light receptor and appears to
425
form long lived radical pairs, which would be necessary for it to work as a magnetoreceptor
426
(Liedvogel et al., 2007). Four different cryptochromes have been found in the eyes of migratory
427
birds, Cry 1a, (Mouritsen et al., 2004, Moller et al., 2004, Niessner et al., 2011), Cry 1b (Moller
428
et al., 2004), Cry 2 (Mouritsen et al., 2004) and Cry 4 (Mouritsen et al., 2004). In terms of figure
429
3, it is thought that the radical pair comprises a flavosemiquinone radical and a terminal residue
430
of a conserved triad of tryptophan residues (a flavin-tryptophan radical pair) (Maeda et al., 2012,
431
Biskup et al., 2009). Based on our understanding of how a similar reaction occurs in plants, the
432
flavosemiquinone radical would appear to lead to the signalling state (Bouly et al., 2007). No
433
direct evidence yet exists however, to demonstrate that cryptochrome is the primary sensing
434
molecule involved in magnetoreception (Mouritsen and Hore, 2012, Liedvogel and Mouritsen,
435
2010). More detailed discussion of the issues around the radical pair compass can be found in
436
(Mouritsen and Hore, 2012, Rogers and Hore, 2009). What is crucial to this review is, does it
437
have a role in the navigational map? All the experiments described above involved disrupting the
438
magnetic compass, in no case was there an indication that the radical pair pathway is involved in
439
map navigation. It does not appear that this mechanism detects intensity, nor indeed the polarity
440
of the magnetic field, only inclination (Ritz et al., 2000). In theory, inclination could be used to
441
detect latitude, so there is no reason why the radical pair mechanism could not be involved in the
442
navigational map, but no experiment has tested this hypothesis. This may be because it could be
443
challenging to design an experiment that is able to disentangle the use of the radical pair sense
444
for a compass from its use in a map.
445
The Ferrimagnetic sense
446
Ferrimagnetic materials are those in which spontaneous magnetization occurs because the
447
magnetic moments of atoms are opposed but unequal. This is seen in iron oxides, including the
448
oldest known magnetic substance, magnetite. Ferrimagnetic material exists in a number of
449
crystalline “domains”, including multi, single and supaparamagnetic. Multi domain magnetite
450
has no magnetisation, single domain has a permanent magnetic moment whereas
451
superparamagnetic magnetite has a fluctuating magnetic moment, but it can be aligned to an
452
external magnetic field (Kirschvink and Walker, 1985). Based on the discovery that bacteria
453
containing single domain magnetite passively align to the magnetic field (Blakemore, 1975), and
454
that magnetite is a biogenic material that is present widely in the tissue of a diverse array of
455
organisms, it was proposed that such material could form the basis of a magnetic sense in multi-
456
cellular organisms (Kirschvink and Gould, 1981, Yorke, 1979). To test this, it was proposed that
457
the physical properties of the ferrimagnetic material could be used to predict the presence of
458
magnetic material in sensory cells in the same way as it had been done in bacteria (Kirschvink,
459
1982). If ferrimagnetic material was involved in a sensory receptor that detected the Earth’s
460
magnetic field then a brief strong magnetic pulse that exceeded the coercivity (the magnetic
461
force required to reduce the magnetisation of the substance to zero) would re-magnetise the
462
substance in the opposite direction if applied antiparallel to the original magnetization (Figure 4).
463
For most biogenic magnetite, the strength required to re-magnetise would be 0.1T, 5000 times
464
the strength of the Earth’s magnetic field (Kirschvink et al., 1985). If single domain magnetite
465
was present it would be re-magnetised, and if used by sensory cells, in theory, would lead to a
466
change in the information the receptor gave. Subsequently, a significant number of experiments
467
have treated birds, with a strong magnetic pulse and indeed found that their orientation is
468
affected by such a pulse. Effects have been found both on migratory birds tested in emlen
469
funnels (BeasonDussourd and Deutschlander, 1995, Wiltschko and Wiltschko, 1995, Wiltschko
470
et al., 1994, Wiltschko et al., 1998), in naturally migrating birds (Holland, 2010) and in homing
471
pigeons (BeasonWiltschko and Wiltschko, 1997). In all these cases a magnetic pulse leads to a
472
deflection in orientation. However, where the pulse was applied antiparallel to the direction of
473
magnetisation, the expected reorientation in the opposite direction did not occur (Wiltschko et
474
al., 2002a, Holland, 2010). This is not consistent with single domain magnetite that is free to
475
rotate in the way a bacteria cell can and does not fit with the popularized concept of a
476
ferrimagnetic sense consisting of tiny compass needles (Mouritsen, 2012). Nor is the fact that the
477
pulse effect appears to be temporary, with birds returning to normal orientation after
478
approximately 10 days (Wiltschko et al., 2007, Wiltschko et al., 1998). This does not support the
479
permanent re-magnetisation of magnetic material. One pulse experiment demonstrated that the
480
deflecting effect of the pulse was removed if the ophthalmic branch of the trigeminal nerve
481
(which innervates the beak) was anaesthetised with lidocane, a local anaesthetic (Beason and
482
Semm, 1996). This suggested that the magnetic pulse effected receptors located in the beak area
483
and the trigeminal nerve was responsible for conveying the input from these receptors to the
484
brain.
485
Two subsequent studies have confirmed the finding that the trigeminal nerve conveys
486
magnetic information. Mora and colleagues (Mora et al., 2004) conditioned homing pigeons to a
487
magnetic intensity anomaly, and found that they could no longer discriminate if the trigeminal
488
nerve was lesioned (although see (KirschvinkWinklhofer and Walker, 2010) for possible
489
weaknesses in the experimental design and (KishkinevMouritsen and Mora, 2012) for failure to
490
repeat the conditioning paradigm). This indicated that the trigeminal nerve was responsible for
491
conveying information on the magnetic field. Following this a study of ZENK expression
492
indicated activation of neurons in the trigeminal brainstem only in migratory robins orienting in a
493
magnetic field that had an intact trigeminal nerve (Heyers et al., 2010). However, homing
494
pigeons that had their trigeminal nerve lesioned were not disrupted in their homing performance
495
(Gagliardo et al., 2006, Gagliardo et al., 2008, Gagliardo et al., 2009). Until recently this made
496
the study of Beason and Semm (1996) the only study to date to indicate a role for the trigeminal
497
nerve in the process of navigation, but what aspect of navigation? Lesions of the trigeminal nerve
498
do not appear to affect magnetic compass orientation in juvenile robins (Zapka et al., 2009), and
499
the pulse deflects the orientation of birds in emlen funnels, but does not affect the magnetic
500
compass (Wiltschko et al., 2006, Munro et al., 1997b). A particular design of pulse experiment
501
however suggests a possible role for the ferrimagnetic receptor in bird navigation. Pulses only
502
appear to effect the orientation of adult migrating birds, not juveniles (Munro et al., 1997a,
503
Munro et al., 1997b, Holland and Helm, 2013), which suggests that the ferrimagnetic sense is
504
involved in an experience based mechanism possessed by adult but not juvenile birds. Since
505
adults have true navigation, this suggests the ferrimagnetic sense is involved in the true
506
navigation map. A recent study has also shown that migrating reed warblers returning to their
507
breeding grounds, are unable to correct for a displacement of 1000km eastwards if the trigeminal
508
nerve is cut, unlike intact and sham operated birds, who are able to do so (Kishkinev et al.,
509
2013). This finding, on migratory birds, is in contrast to the findings on homing pigeons, where
510
no role for the trigeminal nerve in navigation is supported.
511
On this basis it is argued that migrating birds possess two magnetoreceptive pathways: a
512
radical pair mechanism in the eye, which is responsible for at least compass orientation, and a
513
ferrimagnetic sense, which is implicated in the detection of magnetic intensity and is involved in
514
the navigational map (Wiltschko and Wiltchko, 2007). However, caution is urged in accepting
515
this interpretation without question. Adult but not juvenile migratory birds have been shown to
516
respond to changes in intensity (Deutchlander et al., 2012) and adult but not juvenile migratory
517
birds have been shown to be affected by a strong magnetic pulse (Munro et al., 1997a, Holland
518
and Helm, 2013), but there is no direct causal link between the two. Similarly, the trigeminal
519
nerve has been shown to be involved in detecting the magnetic field (Mora et al., 2004), the
520
pulse effect no longer persists when this is anaesthetised, and migratory birds with trigeminal
521
nerve section can no longer correct for displacement (Kishkinev et al., 2013), but there is no
522
direct link between the pulse and magnetic intensity, or the trigeminal nerve and magnetic
523
intensity. Evidence for a ferrimagnetic sense that is responsible for detecting intensity as part of a
524
true navigational map is thus based on several indirect links. We do not know for certain that the
525
pulse affects a receptor that detects intensity, only that it changes navigation behaviour and that
526
the behaviour appears to be mediated by the trigeminal nerve. To be certain of that we would
527
need to know the nature and location of the magnetic receptor.
528
The ferrimagnetic receptor: magnetite or macrophage?
529
Initially, iron-containing cells found in the upper beak of the homing pigeons and other birds
530
were suggested as magnetoreceptors innervated via the trigeminal nerve, although no clear
531
sensory receptor was identified (Beason and Nichols, 1984, Williams and Wild, 2001). A
532
structure that has the potential to be a magnetic receptor has been described in the beak of
533
homing pigeons (Fleissner et al., 2003), chickens (Gallus domesticus), Garden Warblers (Sylvia
534
borin) and Robins (Erithacus rubecula) (Falkenberg et al., 2010). The structure appears to
535
consist of sensory dendrites in the upper beak, which contains iron rich bullets and an iron
536
containing vesicle. It is argued that these are distributed in such a way as to provide magnetic
537
field information in three axes and thus form elements of a magnetometer. Appearing to support
538
the argument that this is a magnetoreceptor, the effect of a magnetic pulse disappears when the
539
upper beak is anaesthetised with local anaesthetic (Wiltschko et al., 2009). The disrupting effect
540
of a magnetic anomaly on homing pigeon orientation also disappears when the beak is
541
anaesthetised (Wiltschko et al., 2010). Again, however, the link is indirect. It is not certain that
542
the anaesthetic is acting directly on the magnetoreceptor in these experiments, and the effects of
543
local anaesthetics have been questioned (Mouritsen and Hore, 2012). A further significant
544
cautionary note to the beak based magnetoreceptor theory has recently emerged. A thorough
545
study made on homing pigeons (Treiber et al., 2012) strongly suggested that the majority of cells
546
identified as containing iron, if not all, both in the upper beak and other parts of the body, such as
547
the skin, respiratory epithelium and feather folliculi are macrophages, cells responsible for
548
engulfing waste and pathogens in the body. Treiber et al. (2012) argue that the structures
549
described in previous work are thus not sensory cells at all. This raises the question of whether a
550
magnetoreceptor exists in the beak. However, the work of Treiber et al. (2012) should not be
551
over interpreted. While the burden of proof is on those who argue that the beak is the site of
552
magnetoreception (Mouritsen, 2012), Treiber et al. do acknowledge that there may be
553
magnetoreceptors in some as yet unidentified location in the beak. Added to this, a number of
554
behavioural studies supporting magnetoreception in the beak have been identified (Wiltschko
555
and Wiltschko, 2013).
556
A second potential site of a magnetoreceptor has also been identified, in the inner ear
557
lagena of homing pigeons, using electrophysiology recordings (Wu and Dickman, 2011, Wu and
558
Dickman, 2012). Recent evidence from electron microscopy has identified iron rich cells in the
559
inner ear (Lauwers et al., 2013), although they do not fit all the properties of a magnetoreceptor.
560
Furthermore, experiments on homing pigeons did not show any deficit in homing with the inner
561
ear removed (Wallraff, 1972), so unlike the beak based sense, behavioural evidence is lacking.
562
Future perspectives: Chronic disease or rude health?
563
As noted at the start of this review, a recent review of magnetoreception suggested that this field
564
suffered from a chronic disease in its lack of repeatability of findings (Mouritsen and Hore,
565
2012). It could be argued that this applies equally to all aspects of bird navigation, with many
566
experiments failing to repeat others, or contradictory results within and between different
567
disciplines. Does this mean that research on bird navigation is in ill health? The assertion by
568
Mouritsen and Hore that experiments must be carefully controlled and designed to avoid
569
observer bias is an important one. However, the recent work of Treiber et al. (2012) that
570
questions the structure and location of magnetoreceptors could actually be viewed as a strength
571
and sign of health: of a field that welcomes new results that may force revisions of current
572
models of understanding. While many aspects of navigation are unresolved, as this review
573
indicates, that does not mean that there is no data. While the models for studying navigation are
574
imperfect, closer links between laboratory work and field work are being established and the
575
addition of new technology for studying animals in the wild will broadened our understanding of
576
the behaviour of migrating birds and the challenges they face (Guilford et al., 2011). The
577
integration of neurobiology, physics and molecular biology into the discipline is now well
578
established and has led to a number of breakthroughs in our understanding of the magnetic sense
579
as well as the role of the olfactory sense in navigation. The integration of these disciplines has
580
led to testable predictions about the structure of sensory systems and potentially the mechanisms
581
of navigation. For the field to advance further, the link between these disciplines and behavioural
582
biology needs to strengthen further, in order to reduce the “black box” understanding of some of
583
the systems involved. For example, a better knowledge of the structure of the ferromagnetic
584
sense will allow better predictions about the effect of magnetic pulse treatments to understand
585
how receptors are changed by the treatment. Strengthening this integration of other disciplines,
586
whilst maintaining the roots as a behavioural biology discipline, will ultimately lead to the
587
solution of the “mystery” of bird navigation. . I will finish this review by highlighting some of
588
the key issues that should be resolved in order for the field of true navigation in migratory birds
589
to advance
590
Key questions in migratory true navigation
591
1) Is the true navigation map unimodal, i.e. one environmental cue provides all information
592
on location, bimodal, i.e. two separate environmental cues provide different aspects of the
593
location (e.g. latitude and longitude), or redundant, i.e. do multiple cues provide the same
594
information for different aspects of the location. Solving this will help to understand
595
some of the inconsistencies and conflicting evidence in the field, as it will establish
596
whether failure to repeat is a consequence of experimental design rather than redundancy
597
of cues.
598
2) Are there one or two magnetic sensory systems with different functions? Clearly
599
establishing whether the magnetite based system is responsible for detecting intensity
600
would establish that not just direction but also other aspects of the magnetic field could
601
be used and form part of the magnetic map.
602
3) Related to 2), can a magnetite based sensory receptor be located and described?
603
Understanding the structure of the magnetoreceptor will help to provide testable
604
predictions for how it might control birds’ behaviour, particularly in light of the pulse
605
experiments.
606
4) To what extent does migratory behaviour in the wild mirror behaviour in an orientation
607
cage? The field of navigation now involves multiple disciplines including those outside
608
biology and requires a controlled laboratory based system that allows predictions to be
609
tested by isolating cues. The orientation cage provides this. However, currently, we have
610
little understanding of how small songbirds respond to displacements in the wild with
611
current techniques being too coarse (ringing, geolocators) or lacking in range (radio
612
tracking). Understanding how songbirds respond to displacements in more detail will
613
indicate the range of their navigation system and thus the extent to which environmental
614
cues will provide reliable information on their location.
615
5) Is “activation” a significant phenomenon within true navigation? The results of some
616
experiments on both olfactory and magnetic cues are consistent with them activating
617
other navigational cues, but this would appear to violate the principle of Occam’s razor
618
by adding another step to the navigation process: If activation plays a part in true
619
navigation, then it moves from a 2 step process (what is my location, what direction to
620
reach home?) to a 3 step process (Am I at home? If no, what is my location, what
621
direction to reach home?), and the two cues providing the most evidence for navigation
622
(olfactory and magnetic) become relegated to intermediate steps towards the actual
623
navigational cues.
624
Acknowledgements
625
I thank John Phillips and two anonymous reviewers for helpful comments on the manuscript.
626
Aspects of this review also came as a result of enjoyable discussions with the Navigation
627
special interest group at the MIGRATE NSF funded meeting in Konstanz, 2010 with
628
Susanna Åkesson, Verner Bingman, Tim Guilford, Anna Gagliardo, Henrik Mouritsen,
629
Rachel Muheim, Rosie Wiltschko and Wolfgang Wiltschko.
630
631
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Figure legends
1008
Figure 1.
1009
Migratory true navigation (A1, A2) is distinct from homing (B) in that the goal is dependent
1010
upon the season. If displaced during the breeding season the animal homes to the same location.
1011
If displaced from the breeding ground during or just prior to migration, the animal will navigate
1012
to the winter ground (A1), or if displaced from the winter ground, to the breeding ground (A2).
1013
Whether this requires different mechanisms or cues that homing has not yet been established.
1014
Figure 2.
1015
In a bi-coordinate map, two gradients (represented by the broad intersecting arrows A and B) are
1016
learned by exploration in the home breeding area. As long as the gradients continue to increase
1017
or decrease predictably, then if a bird is displaced, it can compare the values at the displaced
1018
location with those at the desired goal to calculate the direction of displacement. Only by
1019
learning the values of the winter area can the bird navigate to it, and so migratory true navigation
1020
can only be achieved by adult birds that have made a previous journey.
1021
1022
1023
Figure 3.
1024
A simplified schematic of the radical pair reaction. A photoreceptive molecule forms radical
1025
pairs in the presence of specific wavelengths of light. An applied magnetic field alters the yield
1026
of conversion between singlet and triplet states (yield A vs. yield B in the diagram), leading to
1027
different expression of the signalling state of the molecule (after (Rogers and Hore, 2009)). It has
1028
been hypothesised that this signalling state may be expressed as patterns on the retina, thus
1029
allowing to bird to see the magnetic field, but this has not yet been confirmed (Ritz et al., 2000) .
1030
Figure 4.
1031
Chains of single domain magnetite align with a biasing magnetic field in the direction of
1032
magnetisation (indicated by the red end). Application of a strong magnetic pulse antiparallel to
1033
the direction of magnetisation will re-magnetise in the opposite direction. If such chains are
1034
present in sensory cells and were free to rotate they would give different information about the
1035
magnetic field after such a treatment. In practice however, the effect of pulse treatments on birds
1036
do not clearly indicate that such structures exist.