Navigation In Animals

Animals are capable of true navigation if, after displacement to a location where they have never been, they can determine their position relative to a goal without relying on familiar surroundings, cues that emanate the destination, or information collected during the outward journey (Griffin 1952). Kramer (1957) described the orientation towards a goal which lies outside the sensory range in two fundamentally different steps. Firstly locating the current position with respect to destination, and then orienting in the direction required to reach the destination. This two-step process is known as the Map-and-Compass model owing to analogy with methods of human navigation and can be used to distinguish positional from directional information. However, the ability to navigate in other species does not rely on manufactured navigational instruments but instead upon a variety of different mechanisms available to them through the integration of a number of sensory modalities. Despite the inherent difficulties in understanding the perceptual abilities of different species and how this relates to their spatial representation of the world, it has been possible, through experimentation, to understand the different mechanisms involved in spatial reasoning and their relative importance. This essay will discuss our current understanding first of compasses and then maps in animal navigation, focussing specifically on avian examples. Results from empirical studies will be used to explain the relative importance of the different mechanisms involved which varies according to developmental stage, familiarity with site as well as the sensory capabilities and specific requirements of the species under investigation.

In an unfamiliar environment, there are two reference systems which can be used to gain directional information: geomagnetic fields and celestial bodies. The sun compass was the first of these mechanisms to be tested experimentally. In order to use the sun as a source of directional information, the mechanism must be coupled with the animal's endogenous circadian clock in order to compensate for the sun's movement throughout a day. Therefore, if the sun compass is a necessary source of directional information then it can be predicted that manipulations to the internal clock of an animal will result in a deflection in their bearings. Clock-shift experiments conducted in pigeons, by subjecting them to a phase shifted photoperiod for several days, found that when birds are displaced in unfamiliar locations, they show a characteristic angular shift relative to the correct homing orientation (Schmidt-Koenig 1958). The sun can be distinguished as a source of directional and not positional information because deflections induced by clock shifting were found to depend solely on the amount and direction of the shift, but not the direction and distance of the release. This allowed falsification of the sun navigation hypothesis (Matthews 1953) which posited the use of solar cues for extracting positional information. Whilst the sun compass has been found to be a necessary source of directional information, in many cases it is not fully sufficient to explain correct orientation such as over long distance journeys or on overcast days. Additionally, time compensation mechanisms must be tuned to the sun's local arc in the home region meaning that the sun compass is based on experience (Wiltschko et al. 1983). This therefore requires an alternative innate compass mechanism as a reference.

The sun compass is probably based on visual input of the eyes, but it is still unclear where this input is combined with the internal clock to derive directions. Birds extract directional information from the sun using it's azimuth, the angle of the sun from due north in a clockwise direction with respect to a target destination, whereas its altitude is neglected. The light from the sky is partly polarized, therefore theoretically at least allowing a mechanism of determining the sun`s position when the sky is partly cloudy. Whilst polarization is known to be used in insects, it is not clear to what extent it is using in homing birds. In migratory birds, the polarization pattern appears to play an important role at sunset, when many night-migrating birds start their nocturnal flight. In Blackbirds it was found that at sunset, individuals will prefer the correct migratory direction until their cage is covered by a depolarizer that eliminated polarization.

A compass mechanism based on the geomagnetic field was first described in the European robin whose migratory behaviour could be disturbed by shifting the magnetic field. Birds were tested in Emlen funnels which can document the dominant direction of movement with magnetic north shifted. The orientation behaviour of these migrants was found to shift predictably with the magnetic field clearly indicating the importance of geomagnetic cues in integrating directional information. Further experiments found that the magnetic compass differs from a technical compass used by humans in that it does not respond to polarity and instead gives bearings relative to either pole or the equator rather than north or south. Bird rearing experiments with altered magnetic fields indicate that the magnetic compass is an innate mechanism and has therefore been proposed to form the first means for navigation and homing in birds and serve as a directional reference for the learning processes required to establish the sun compass (Wiltschko, et al., 1983). Clock shifted experiments with pigeons carrying magnets indicate that in mature birds, magnetic and sun compass systems are used together with both contributing to the decision of which direction to fly. For some decades after this discovery that birds can derive directional information from the geomagnetic field, the nature of this magnetic sense remained enigmatic, and the lack of knowledge on magnetoreception caused considerable skepticism. However, in the past decade findings have elucidated much of detail involved after discovery of the underlying radical pair mechanism on which magnetoreception is based. This mechanism proposes that the earth`s magnetic field alters the unpaired electron spin state of photoreceptive chemicals in the eye, most likely cryptochromes. Magnetic compasses are phylogenetically widespread and exist in several invertebrate groups, as well as in all major groups of vertebrate animals.

Most research on magnetoreception has focused on the directional information that can be extracted from the Earth`s geomagnetic field, as described above. However, the field varies predictably across the surface of the globe, meaning that it also provides a potential source of positional information. This ability to use positional information derived from the Earth's geomagnetic field is known to be important in long distance migrations of a number of taxa. The Pied flycatcher (Ficedula hypoleuca) is one example of a migratory bird which potentially uses this information to change direction to avoid ecological barriers. The central European population of pied flycatchers begins its migration by flying southwest to Iberia, after which it changes to a southeasterly course. This two-step migratory pathway enables the birds to avoid the Alps, the Mediterranean Sea, and the central Sahara. Experimental evidence using captive birds has found that individuals exposed to a sequence of magnetic fields approximately matching those they normally encounter while migrating resulted in a shifted orientation in the same direction as expected natural migration. Directional shifts did not occur in birds which were exposed to the ambient field suggesting that the birds must detect the field change at specific locations at the appropriate times in order to orient appropriately during migration (Lohmann & Lohmann, 2006). Additional evidence from both loggerhead and green turtles has also implicated magnetic cues in map-based systems; however this tentative mechanism of goal navigation is still lacking direct evidence and remains highly controversial.

One proposed mechanism for detecting gradients in the magnetic field and therefore allowing the use of map-based navigation involves a receptor using ferrimagnetic material. This mechanism can be experimentally disrupted by applying a strong magnetic pulse that re-magnetizes ferrimagnetic materials which affects the bearings of treated individuals. In order to distinguish the effect of this treatment on map and compass mechanisms, one study using European robins (Erithacus rubecula) compared the orientation of juvenile and experienced adult birds when subjected to a magnetic pulse and released from a migratory stop off site (Holland & Helm, 2013). It was found that precision of departure direction was affected in adults but not juvenile birds. Therefore, it has been argued that because only adults can rely on experience based map information, the pulse is affecting a receptor that is involved in detecting the Earth`s magnetic field to be used specifically in the navigational map mechanism. An alternative navigational explanation could be that the ferrimagnetic sense has different roles in the adult and juvenile magnetic compass systems, or that the ferrimagnetic sense may also play a role in the magnetic compass. This study has been replicated using pigeons and found no effect of magnetic pulse on homing ability which therefore does not support a role for the ferrimagnetic sense in homing pigeon navigation. Whilst the links between the behavioural aspects of magnetoreception and the neurobiology of navigation remain unclear, the importance of magnetic cues in experience based mapping continues to be strongly debated.

Olfaction and vision are two sensory modalities which are more widely accepted to be used by navigating animals in order to gain positional information. Olfactory chemicals form gradient maps which can be distinguished from mosaic maps which involve the spatial relationships between familiar landmarks because they allow goal finding from unfamiliar areas. If these gradients extend monototically beyond the familiar area, scalar values of the chemical concentrations at the current position, as compared to those remembered at the home, can be used to gain positional information. In order to provide accurate positional information at least two gradient fields must intersect at sufficiently large angles. Theoretically, this seems improbable as weather conditions such as temperature and winds will hugely affect odour concentrations introducing much stochastic noise. Additionally, the physiological requirement to accurately perceive relative concentrations in the same modality appears unlikely. Olfaction may not act here as a classic sensory modality in the way that it has been characterised in humans but instead may be perceived in a similar manor to the magnetic sense.

The exact role of olfaction remains the source of some controversy; however numerous experiments on anosmic birds indicate a key role for this type of mapping in avian navigation. Intranasal irrigation with a solution of zinc sulphate is one such method of olfactory deprivation which can be used to test the navigation ability of treated birds relative to controls. In familiar areas, homing ability is not affected by this treatment, presumably due to reliance upon visual cues which will be discussed shortly. However, homing success was greatly reduced over longer distances in unfamiliar areas. This is a result which has been replicated in various regions of the world in pigeons and therefore leads to the conclusion that homing from unfamiliar locations is substantially influenced by olfactory perception (Walraff, 2010). Alternative interpretations of these results however include the possibility that birds use their sense of smell to correct for wind drift or to avoid the coast.

A number of experiments were carried out in order to test how pigeons obtained olfactory maps from development. It was found that when reared with visual cues but without exposure to wind, pigeons show the same impairment in orientation and homing described above. By manipulating the direction of winds with deflector panels it was also found that pigeons only orientate towards home from a direction when they had been exposed to winds heading in that direction (Papi, 1992). This led Papi to conclude that each wind carries information useful for homing from the direction it blows and that birds build up a map of different olfactory gradients in their early development. It has been argued, however, that the use of wind deflector panels will not only change wind direction but also light cues which are proposed to form part of a light-based reference system derived from polarized light patterns used to calibrate the avian sun compass (Phillips & Waldvogel 1988). The acquisition of this stored information apparently requires activation by olfactory input. This olfactory activation hypothesis therefore suggests that natural odours are not the basis for site-based map information. A recent study designed to distinguish between olfactory activation and olfactory map hypotheses compared homing ability in young inexperienced birds exposed to novel odours containing no positional information with those exposed to natural odours finding no significant difference between treatment and control (Paulo, et al., 2010). Whilst this appears to provide evidence for the olfactory activation hypothesis, the mechanism by which this might occur has not yet been characterised.

Visual cues provide the most obvious and perhaps the least controversial mechanism for perceiving spatial information. This mapping mechanism is thought to be based on a learned mosaic of landmarks and is therefore dependent upon the individual's experience. Clearly, visual landscape features can only be helpful within an area that has been explored during previous flights and therefore this mechanism is effective over a much more restricted range than olfactory mapping. Impairment of the visual system so as to exclude possible use of landmark cues but also not impair flight itself is problematic. One experiment found that pigeons wearing frosted lens took less direct routes home than controls, however this could be attributed to general behavioural disturbance (Schmidt-Koenig & Schlichte 1972). Direct positive evidence for the use of visual features of the landscape is hard to obtain and therefore the exact mechanism by which these landmarks are use remains unresolved. Direct evidence might most convincingly be obtained with a demonstration of shifting landmarks corresponding to a predictable shift in orientation behaviour, however pragmatically this may not be possible in natural environments. An alternative approach was adopted by Gagliardo et al. (2001) who used preview and escape experiments with anosmic and control birds which were either allowed preview the environment or were hidden before release at familiar sites. The anosmic group that was denied a view of the landscape on release was not oriented at the point of escape from the arena, whereas the control group was. Anosmic birds with visual access were well oriented in the home direction at the point of escape demonstrating that visual cues could be used to orient in the absence of olfactory cues. It was argued therefore that this result provides direct evidence for the use of visual cues in navigating from familiar sites. One significant question which could not be resolved from the study above is whether the landmarks are used independent of the map and compass mechanism. A mosaic map, as described above, is one in which compass bearings from landmarks are used. Alternatively, pilotage describes a mechanism independent of Kramer's Map-and-Compass model where visual landmarks provide a direct progression towards a goal, therefore defining the route without directional information. Piloting, a mechanism originally proposed by Griffin (1944), is a mechanism which had been largely dismissed until modern GPS systems made it possible to record the tracks of returning pigeons with great accuracy. Biro et al. (2004) found that the routes of birds repeatedly released from the same sites were found to become stereotypic after around 10 flights which can be attributed to navigation by following sequences of familiar landmarks. The use of a sun compass in these instances of familiarity was tested using clock shifted experiments to look for deviations in expected direction. It was found that clock shifted individuals do show a deflection orientation leading to the conclusion that pigeons combine compass and landmark information in familiar areas (Biro, et al., 2007).

This essay has discussed the principle sensory cues involved in avian navigation and the mechanisms by which they are used. Despite debate over the relative weight given to various cues in different levels of familiarity and for different navigational tasks, Kramer's Map-and-Compass model remains useful for studying and categorising different mechanisms. Both directional and positional information, although derived independently, must be integrated in the brains of birds to form a spatial perception of the world, which, by definition, will always be hard for humans to fully understand. The way in which spatial knowledge is stored neurologically is largely unknown and will form an interesting dimension to a full understanding of animal navigation. It is not surprising that there is apparent redundancy within navigation systems, with multiple mechanisms for each task, as this will clearly be adaptive in a world which is subject to change. For this reason, it is also not surprising that navigational mechanisms rely on both innate and learnt components providing different information depending on the development and maturity of the animal. This combination of innate and learned components makes the navigational system highly flexible. The innate components allow navigation before the experience-based ones are established and provide the opportunity to acquire the necessary experience therefore making the avian navigation powerful and effective.