The environment presents periodic alterations, in the seasons and over the days; animals, in order to survive, must be able to adapt to them and sometimes to anticipate them. Equally adaptive are the ability to perceive the duration and succession of events [1] , thanks to which, for example, it is possible to react in time to a predator [2] . In general, the perception of time is fundamental for the regulation of physiological mechanisms , for synchronization with environmental alterations and for intra and interspecific interactions [1, 2] .
It must be remembered that temporal perception, like all physiological activities, has energy costs ; these are particularly high the faster the stimuli to be perceived are. Therefore the resolution of the temporal perception (that is the minimum temporal unit with which the stimuli vary) will be different according to the ecological , environmental and intrinsic factors to which the species is subjected. Simplifying, we can say that resolution will always be the bare minimum for that species [2] .
For example, we can verify that the perception of the passing of hours in the day is an adaptation to environmental changes if it is absent in species that have few environmental influences. Heterocephalus ( Heterocephalus glaber ) are mammals that almost always live in the darkness of tunnels dug into the ground: they therefore do not have to face periodic environmental changes. From the experiments it emerges that their activities occur randomly during the day, without following daily cycles [3] .
Let’s analyze the temporal perception of animals, according to the perception capacity of the passage of time, temporal durations, succession of events, periodicity and rhythms.
The perception of the passing of the days
What does the passage of time indicate to animals? The alternation of hours of light and darkness provides temporal indications , as it reflects the passing of the days. House rats ( Mus musculus ), for example, “count” days based on the times when light is present or absent over long periods of time.
Male rats once mated become very violent towards any pups they encounter. They become less and less aggressive, however, until three weeks pass after the last copulation, when the infanticide behavior ceases. It is the moment in which their partners give birth, so if they were still aggressive they would risk killing their puppies: it would be a non-adaptive behavior.
How do we know that aggression in these animals is regulated by the alternation of light and dark? If kept in a laboratory where light periods are shortened, the infanticide behavior ceases sooner. The perception of the passage of time is therefore altered as a consequence of the duration of the periods of light [3] .
Each species perceives the speed of time differently depending on its metabolism and body mass. For example, the cat ( Felis catus ) perceives time more slowly than a rat ( Rattus norvegicus ). This can be explained as follows: for physical reasons larger animals are slower in their movements, so a high time resolution would involve unnecessary costs. It is therefore possible that natural selection has negatively selected this ability in large animals [2] .
The perception of the temporal duration of events
Even non-human animals are capable of internally representing the duration of events. An example of this ability is demonstrated in Church and Gibbon’s 1982 experiment. Rats, kept in the laboratory, had to push levers to get food as a reward. This, however, was only given if the lever was pressed after a dark interval of 4 seconds. The animals were able to correctly estimate the length of time, pressing the lever only when the length of time was the “required” [1] . Pigeon (Columba livia), parakeet ( Melopsittacus undulatus ), diamond mandarin ( Taeniopygia guttata ) and other animals are also sensitive to changes in the duration of signalsto their subordinates [4] .
The perception of the succession of events
A simple example of how other animals are able to grasp the sequence of events is found in conditioning experiments , as they require individuals to associate stimuli with responses that follow them. Among these is known the experiment of the physiologist Pavlov who taught dogs to associate the sound of the bell with the arrival of food [1] .
Another example is given by experiments in which the animals are trained to touch entire sequences of stimuli (e.g. first A, then B, then C, finally D) and then it is observed whether they are able to connect the intermediate ones (e.g. only B , C or just C, D). The cebi (subfamily Cebinae ) and the pigeons ( Columba livia ), for example, have shown themselves capable [1] .
The periodicity of the environment and the biorhythms
The biological functions vary cyclically every day, as in the sleep-wake rhythms; every month, as in the case of menstruation in Homo sapiens ; every year, for animals that breed once a year or migrate. But heartbeats, motor activities and the production of some hormones also require regular cadences [1] . The ability to produce periodic movements is therefore universal in vertebrates [4] .
Sometimes the internal representation of time is physiologically automated. This was first observed in 1922 by Richter. In fact, he reports that rats had regular sleep-wake rhythms even in conditions of perennial darkness [1] . The periodic timing of the body’s functions is attributable to biorhythms , also called biological clocks, which can be:
- high frequency rhythms , with very short periods. Examples are that of the discharge of action potentials in neurons and that of cell division [1] ;
- rhythms synchronized with natural periodicities [1] , also called long-term behavioral cycles [3] . There are five main natural periodicities and as many types of biorhythms follow.
Long-term behavioral rhythms
Biorhythms with a periodicity greater than 28 hours are called infradians, while those with a rhythm of less than 20 hours are called ultradians. The main long-term behavioral cycles, however, are the following.
- Annual rhythms : they are in sync with the calendar year, so they are equivalent to about 365 days. This biorhythm allows you to concentrate behavioral activities such as reproduction, hibernation and migration at the most appropriate time of the year.
- Lunar rhythms : synchronized to the lunar cycle, with a period of 29.5 days. These biorhythms occur in animals that exploit the tides to reproduce and in other animals that, for example, avoid bright nights, in which they would be more visible to predators, such as the tuft-tailed kangaroo rat ( Dypodomis spectabilis ).
- Semilunar rhythms : they are synchronized with the alternation of sigizial tides, ie the deepest low tides. They occur on the occasion of the full moon and the new moon, with a periodicity of 14.8 days.
- Daily rhythms : in sync with the alternation of day and night, they last 24 hours. Many animals have this biorhythm, which influences numerous behaviors (such as birdsong at dawn) and physiological mechanisms (such as the release of hormones);
- Tidal rhythms : synchronized with the high and low tides, which occur each twice a day. Their period is therefore 12.4 hours. It occurs in animals that have to anticipate low tides, such as some crabs that take refuge among rocks or in the sand to avoid being exposed to air or predators [1,3] .
The rhythms listed above take the name of circannual , circalunar , circasemilunar , circadian (from dies , “day” in Latin) and circatidal in aperiodic conditions , or in the absence of the periodic environmental phenomenon with which they are synchronized. In fact, in constant light or dark conditions and unchanged temperature, biorhythms manifest themselves equally, albeit in an approximate way. The new rhythm is called spontaneous and also demonstrates the endogenous nature of long-term behavioral rhythms [1,3] .
Spermophilus lateralis photo. Shared under the Creative Commons CC0 license .
This is the case of the rats of Richter’s experiment reported above: they have a circadian rhythm even in constant conditions [1] . Another example is that of the golden ground squirrel ( Spermophilus lateralis ), which in an experiment has maintained its circannual rhythm over the years despite being in constant laboratory conditions [3] .
The circadian rhythm is called freerunning as it partially deviates from the periodicity it shows in nature. Depending on the species, in constant conditions this periodicity can be from 21 to 28 hours. This genetically determined variation allows the animals to adapt to the change in the length of the day throughout the year. The phenomenon is studied in special cages where the activity of the animal is recorded, according to the time of day, by means of traces called attigrams [1] .
How does synchronization with environmental factors take place?
The “circa-” rhythms are however partly sensitive to the environment, so that they can be continuously adjusted according to changes in natural rhythms [3] . Consequently they can be altered by changing the periodicity of some environmental factors. For example, by varying the periods of light and dark: the synchronization to the latter is called photic entrainment . There are also non-photic entrainments , such as the thermal one [1] .
Entry systems must consist of three components to function. The first is an input path , through which the environmental stimulus can be perceived by the individual. The second is a pacemaker , a structure that generates the rhythm. The third is an output path that determines the expression of the rhythm by conveying the information from the pacemaker to the central nervous system. These physiological pathways are generally studied by means of ablation , ie the surgical lesion of structures: if variations in behavior are observed, that structure was useful in determining it [1] .
In the case of photic entrainment, the input path is generally the retina, the pacemaker is the pineal gland and the output path is the suprachiasmatic nucleus (a hypothalamic structure). In short, the perception of light inhibits the production of the hormone melatonin which, among its functions, regulates the rhythmicity of the body and promotes sleep. In the path of this information, however, there are great variations even among species that are very close phylogenetically [1] .
The perception of light is also fundamental to determine the time of the year in which the animal is. In particular, the photoperiod (number of hours of light in a day) is an indicator of the current season. For example, white-crowned sparrows ( Zonotrichia leucophrys ) have a strong reproductive seasonality. A photoperiod of over 14 hours indicates to this animal the arrival of spring, causing hormonal changes that lead to the development of the gonads. This happens because the photosensitivity of the animal is practically nil before 14 hours from the start of the day, so a lower amount of hours of light has no effect on the photosensitive physiological systems [3] .
The genetic basis of biorhythms
The circadian system is based on the clock genes : per (period), tim ( timeless ) and clock (clock). Simplifying a lot we can say that these genes produce proteins that accumulate in the body throughout the day, influencing the sleep-wake rhythm of individuals [1] . The gene for , in particular, seems to play a very important role. In humans, for example, a gene mutation for causes significant sleep disturbances: these people fall asleep around eight in the evening and wake up before five in the morning [3] .
Another example of the importance of the gene for is observable in honey bees ( Apis mellifera ). The young usually stay inside the hive almost all day, taking care of the larvae and eggs. The older ones, on the other hand, forage during the daylight hours. The production of PER proteins (derived from the per gene ) is very different: older bees produce about three times more than young bees [3] .
The gene for is therefore very old: it is thought to date back to a common ancestor of mammals and insects that lived 550 million years ago [3] .
Perception of “musical” rhythm in animals
A rhythm can be defined as a succession of time durations marked by events such as sounds (called units) and silences (called intervals) [5] . The perception of rhythm is a consequence of the combination of a series of factors, including the ability to represent one’s own biorhythms and the ability to synchronize with the rhythm of perceived sounds. Many studies suggest that the neural basis of rhythm perception involves brain regions associated with motor functions [4] .
Animals that perceive the rhythm are mainly among primates and birds. For example, man, gorilla ( Gorilla gorilla ), chimpanzee ( Pan troglodytes ) and bonobo ( Pan paniscus ) show a spontaneous behavior that requires rhythmicity: drumming, or beating time with the paws on your body or on objects. Another example is observable in animals capable of moving in time, even changing it when the rhythms subjected to them vary. Among these animals are some species of rats, parrots, elephants and seals. Other capabilities subordinated to rhythm, such as synchronization with the movements of conspecifics, are even more widespread in the animal world: for example, some frogs, crickets and fireflies show them [4,5] .
The perception of rhythm essentially occurs in social animals. Rhythm is in fact fundamental to communication, whether it is vocal or other behaviors. As for the singing birds and in the Indri indri lemurs , where rhythm is a very important component of vocalizations [5] . The perception of rhythm assumes a strong adaptive value where synchronization of individuals of a species is necessary , as in the case of the courtship display of male fiddler crabs (belonging to the genus Uca ). These, in fact, during the courtship of the females wave their claws in synchrony [4] .
In man, in particular, it is observed that synchronization (as in dancing, singing and dialogue) can play a role in the formation and intensification of social bonds [