How to tell time

Light-dark rhythm (photoperiod) is known to regulate production of the hormone melatonin that, in turn, regulates circadian (meaning around a day, as in a 24-hour period) rhythms by a feedback mechanism. In surface-dwelling vertebrates (including human), melatonin is produced during dark hours. It can therefore be expected that subterranean mammals living in constant darkness would display high melatonin levels. This does seem to be the case, yet the role of melatonin in regulating activity rhythms in subterranean animals remains obscure.

Permanent darkness in subterranean burrows makes sight and eyes rather useless and, apart from the fact that it precludes visual orientation in space, it also makes orientation in time problematic. Virtually all surface-dwelling mammals exhibit more or less pronounced circadian cycles of activity and diverse functions. These cycles are maintained by an endogenous pacemaker synchronized (entrained) by the so-called zeitgeber (time-giver). The most universal zeitgeber is the light-dark cycle perceived by photosensors. Considering the stability of the environment, constant availability of plant food, darkness underground, and poor sight or even blindness, one might expect that herbivorous subterranean rodents would not exhibit distinct diurnal activity/sleeping patterns. Field and laboratory studies on American pocket gophers (Geomys bursarius and Thomomys bottae) and African mole-rats (Heliophobius argenteocinereus and Cryptomys hottentotus) have revealed dispersed activity occurring throughout the 24 hours, for instance, arhythmicity and lack of distinct sleep-wake cycles. Interestingly, there are some other species of subterranean rodents that exhibit endogenous circadian activity rhythms that are free running in constant darkness and synchronized by light-dark cycles. These animals have been found to be either mostly diurnal such as the east Mediterranean blind mole-rat (Spalax ehrenbergi species complex), the East African mole rat (Tachyoryctes splendens), and the Kalahari mole-rat (Cryptomys damarensis); or predominantly nocturnal such as the African mole-rats (Georychus capensis and Heterocephalus glaber) and the Chilean coruro (Spalacopus cyanus).

There is no apparent correlation between the circadian activity pattern, on the one hand, and the degree of confinement to subterranean ecotope, development of eyes, sea-sonality of breeding, or social and mating systems, on the other. It should be noted, however, that findings in the same species have frequently been inconsistent. Available data have been obtained by different examination methods and may not be fully comparable. Moreover, there may be differences between individuals, sexes, and populations, between seasons of the year and habitats, as well as between the laboratory and the field. The methodological problem can be demonstrated in the example of the naked mole-rat, which had been considered to be arrhythmic by previous authors, yet was shown to display clear circadian rhythms and ability to synchronize them by the light-dark cycle if given an opportunity to work on a running wheel in the laboratory. There is a similar finding in Cryptomys anselli. Further studies of activity patterns in other species of mammals are clearly needed. A possible zeitgeber determining digging activity can be also temperature and humidity, which may fluctuate in shallow tunnels (although certainly not in deep nest chambers), as well as consequent changes in activity of invertebrates, which may affect foraging activity of moles.

The blind mole-rat, which is visually blind and has degenerated eyes, still has a hypertrophied retina and a large harderian gland in which the so-called circadian genes as well as the recently discovered photopigment melanopsin are expressed in high concentrations, and these apparently contribute to regulation of photoperiodicity. In other words, the double function of any vertebrate eye changed: instead of sight and circadian functions, only a circadian eye remains.

The ability to perceive and recognize the length of the photoperiod is important for seasonal structuring of reproductive behavior. It has also been suggested that melatonin may suppress production of gonadotrophins, hormones which, in turn, control activity of gonads and, thus, the sexual behavior and reproductive biology. Nothing is known about this aspect in subterranean mammals. Also unclear is how circannual (approximately one year) cycles are synchronized in subterranean mammals. These cycles are associated particularly with seasonal breeding in solitary territorial animals. It is assumed that the length of the photoperiod may play a role in seasonal breeders from temperate zones. Nevertheless, factors triggering breeding in mammals with long gestation from the tropics (where there is minimal variability in the daylight throughout the year) remain unknown and enigmatic in many cases. This is also the case for the eastern African silvery mole-rat. Alternating rains and drought represent the main periodic environmental factor. However, as shown recently, mating takes place at the end of the rainy and beginning of the dry season so that there is a substantial lag between the onset of rains (and subsequent softening of the soil and change of vegetation that could provide a triggering signal) and onset of breeding behavior.

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