Orientation is essential for most animal species. According to the definition given by Treccani, animal navigation is ” the ability of an animal to reach a spatially defined and limited destination, even relatively far away “. Therefore, it does not include shifts towards an already perceptible destination (visible, odorable, etc.) upon departure, for example those that occur within the range of action of echolocation [1] .
In most cases, the animals reach already known places, a phenomenon called homing (which can be translated as “homecoming”) even when they do not return to their nest [1] . This can be done simply by reversing the direction ; through automated mechanisms; or through true navigation , or the ability to find the right route even in unknown places and without any reference, thanks to the integration of different navigation systems [2] . Animals capable of true navigation are therefore able to compensate for passive displacements, ie human movement of the animal – a method used in experiments investigating the orientation skills of animals [1] .
Two parameters are essential for an animal to move:
- that has reference points available . These can be external (allocentric) or ego-centered, ie measurable by the animal on the basis of its own movements [2] ;
- the sense of time : a biological clock (ie the set of physiological mechanisms that determine the rhythm of the organism’s activities) [2, 3] .
Types of animal orientation
It is on the basis of the exploited landmarks that the ways of navigating animals are categorized. There are four different types of orientation in space : the use of compasses (astral or physical reference systems); the use of landmarks (environmental reference points); the use of mind maps; and dead reckoning (estimation or recording of the route taken). Only in emergencies do animals orient themselves by resorting to random explorations [2] .
Compasses
The compass orientation is a navigation mechanism dependent on the presence of stars or referred to the earth’s magnetic field. Animals capable of compass orientation have the innate ability to understand the direction from which a certain point of reference is coming and to be able to orient themselves accordingly [1] . There are four types of compass orientation.
Solar compass
The Sun, in the sky, “moves” about 15 ° every hour. Therefore to refer to it as a reference point it is necessary to consider that it is not always in the same position during the day. Animals that have a solar compass are those capable of orienting themselves by compensating for the movement of the sun over time , such as starlings (Sturnus vulgaris). If you keep a starling in the laboratory where a lamp simulates the presence of the Sun, you can observe that the direction in which the animal flies changes throughout the day. The reversal, in fact, changes its position with respect to the angle of the lamp to compensate for the displacement of the Sun that occurs during the day [2, 3] .
Another example is that of doves or wild pigeons ( Columba livia ), which tend to fly in the direction of their own dovecote. If you bring some of these animals into the laboratory, changing the alternation of light and dark of the lamps, it is possible to manipulate their biological clock so that it is six hours out of phase with the Sun. By releasing the pigeon it will try to reach its own pigeon house; suppose this is to the east. At six in the morning the pigeon would fly in the direction of the Sun; but with the internal clock out of phase, say, by six hours, the bird would perceive the Sun as being noon, so it would move northwards [3] .
Warning: using the Sun as a reference point does not mean having to see it . How do animals perceive it? One way is to refer to the projection of the Sun, the azimuth [1] . Another way is through the light itself, in particular its polarization , that is the phenomenon to which it is subjected when it passes through the atmosphere that causes the wavelengths to vibrate only on a plane perpendicular to the direction of the sun’s rays. In other words, the “rays” of the Sun are filtered by the atmosphere in order to have precise directions, which change as the star moves. Animals that exploit this system are, for example, monarch butterflies ( Danaus plexippus ) [1, 3] and some Chiroptera [4] .
Lunar compass
Animals with a lunar compass endogenously compensate for the motion of the moon in the sky , similarly to the solar compass. The talitro or beach flea ( Talitrus saltator ) uses the lunar compass and is also an example of how, frequently, animals have more than one type of compass orientation. In fact, they also have a solar compass [2] .
Star compass
It is used, in particular, by migratory birds that migrate at night [2] . In the laboratory, it is possible to change the direction taken by these animals simply by rotating the planetarium over them [1, 2] . It seems that this type of navigation is subordinated to the recognition of circumpolar constellations . In fact, in an experiment, it was observed that the birds of the Passerina cyanea species become unable to orient themselves when the constellations within 35 ° of the polar star are obscured [1] .
Geomagnetic compass
When it is not possible to refer to the stars – for example in the depths of the sea – it is possible to resort to the Earth’s magnetic field , or the set of magnetic forces generated in the core of our planet. Green turtles (Chelonia mydas), for example, change their direction of navigation if the magnetic field changes. This was verified by immersing them in tanks surrounded by magnetic coils that were manipulated by computers (in a study by Ken Lohmann and colleagues from 2004: “ Geomagnetic map used in sea-turtle navigation ”) [3] . Bogong moths ( Agrotis infusa ) [4] and several birds as wellthey modify their movements according to variations of artificial magnetic fields in which they are inserted. The physiological mechanism behind this type of orientation is still unknown [2] .
The use of landmarks
The use of environmental references (landmarks) for animal orientation derives from stimulus-response associations: individuals learn to link the presence of a clue present in the environment (for example) to food or other positive reinforcements [3] . Navigation based on landmarks is called piloting ; it can be visual, olfactory, tactile depending on the type of stimuli that drive it [2] .
For example, gerbils (Gerbillinae, a subfamily of the Muridae) are capable of this. In one experiment they were used to finding food at the center of three reference points. When one or two of these were removed, the gerbils searched for food at points around the residual landmark corresponding to what would have been the center of the initial triangle [2] . Another example of the use of landmarks was observed by Tinbergen on the terraiola wasp , the family of wasps Sphecidae.
This type of orientation is particularly important for animals that stock up on food (and consequently have to hide it). As in the case of the Clark’s nutcracker ( Nucifraga columbiana ), a bird that hides up to 33,000 seeds in autumn that it will recover over several months; however, it also benefits from cognitive maps [2, 3] .
Cognitive maps
Some animals, such as Homo sapiens , are able to form cognitive maps, or mental representations of the relationships between all the objects present in a given place . As a consequence of the formation of a cognitive map, the animal is able to orient itself even if it is moved or if some environmental clues are removed [2] . Animals using this orientation method include vertebrates, such as rats, and invertebrates, such as bees [2, 3] .
The creation of mental maps within the memory of individuals is a passive and spontaneous phenomenon, independent of the presence of reinforcements (unlike the use of landmarks ): it is a form of latent learning , which therefore occurs automatically. For example, rats are able to take advantage of shortcuts and circumvention strategies in mazes with blocked channels, even if they have never been reinforced to do so [2] .
The American Bigie tits ( Parus atricapillus ) store the food at certain points of the ground and then return there after one or more days. In experiments where these storage sites are covered and emptied, birds look for food in the places where they buried it, even if there is no odor or visual indication to that effect. This shows that they remember where they sowed it [3] . Further proof of this is that when the experimenter hides the food these birds are unable to find it [2] .
Mind maps and hippocampus
Alaskan gray tits store far more food than the Colorado conspecifics to cope with the intense cold they are also much quicker to spot previously hidden food. Both in the Alaskan gray tits, compared with those of Colorado, and in humans, the greater mnemonic ability of cognitive maps is reflected by the greater dimensions of the hippocampus , a brain structure that responds to experience. In fact, in Homo sapiens it has been seen that London taxi drivers have a hippocampus larger than that of men who carry out a different job, which does not require to remember the map of a city [3] .
In particular, two types of hippocampal neurons are involved in the mechanism of cognitive map formation: place cells and head-direction cells . The former are activated according to the position that the animal occupies in space; the latter, on the other hand, discharge when the animals’ heads are oriented in a certain direction. The origins of this nervous structure are thought to date back to the common ancestor of birds, mammals, reptiles and Actinopterygii (ray-finned fish) [2] .
The dead reckoning
When the reference points are not many, it is possible to observe another type of orientation behavior of the animals: dead reckoning (which can be translated as “blind estimation”). This mechanism consists of the ability to calculate where the starting point of your journey is based on the distance and angles traveled . The animals that implement it record their own path, calculating it (unconsciously) thanks to the vector sum of the directions traveled and the angles with respect to a reference point such as the Sun.
It is therefore a more complex phenomenon than the simple reversal of direction, practiced for example by paper wasps (of the genus Polistes ) [2] . The dead reckoning is hardly noticeable by itself [2] , as is generally supplemented by clues such as odors, geomagnetism, vibrations [5] .
An example of dead reckoning animals are desert ants (genus Cataglyphis ). These arthropods live in anthills dug into the ground. When they move away from the nest they explore the territory around them in search of food, reaching hundreds of meters in disorderly paths. The return, on the other hand, takes place in an almost straight line: the shortest route, regardless of the deviations of the outward journey [2] ( see figure 1, b ). How do we verify that this does not happen thanks to mind maps or the use of compasses? If the ant is moved after finding the food, it will move in the same direction it would have had had it not been moved ( see figure 1, ced). For example, if during its return to the anthill we place it 5 meters to the west, it will arrive 5 meters west of its anthill [2] .
Figure 1: the dead reckoning. (a): outward, exploratory path. (b): return path, linear. (c) and (d): return path following passive displacement. Image created by Jolanda Serena Pisano for BioPills, freely taken from J. Alcock, 2017, and Sovrano VA et al., 2009.
Another example of animals capable of dead reckoning is that of honey bees: to verify this, an experiment can be performed. First of all, the bees get used to following a precise path to reach a certain point (eg sugar water supply points), which will be in a specific direction and distance from the hive. Bees will be able to follow the right direction, without hesitation, even when experimenters move the hive. Unlike desert ants, however, bees find the exact spot because they also have a solar compass. They immediately find their way back even when they are locked up for three hours (with a consequent delay on departure) because, physiologically, they compensated for the 45 ° shift of the Sun that occurred while they were locked up.
