This paper discusses intraspecific variations and interspecific differences in the “hibernation zone” and the mechanism of its formation on the incisor surface in three groups of rodents with different hibernation patterns: marmots, ground squirrels, and hamsters. The incisors of these animals continue growing during the hibernation period. Marmots and ground squirrels do not feed during hibernation; accordingly, the mechanical stress on their incisors differs significantly prior to, during, and after the hibernation period. During hibernation, the incisor growth rate is minimum, and a “hibernation zone” is formed on the incisor surface. In marmots and ground squirrels, this zone has two common features: very narrow increments and changes in the enamel–dentin junction. The interspecific differences between marmots and ground squirrels in the “hibernation zone” patterns can be attributed to regional differences in the climate. Hamsters can feed during hibernation. Their incisors grow more significantly, and the enamel–dentin junction on the incisor surface does not change. Thus, the “hibernation zone” is distinguished only by narrower and more distinct increments in comparison with daily ones. The interspecific differences between hamsters in hibernation records can be significant, up to the complete absence of such records. Apparently, these differences are determined not as much by climate as by differences in the hibernation patterns.

As was shown earlier, in some hibernating rodents the patterns of hibernation are recorded by tooth dentine and can be revealed in stained or ground sections of the incisors, as well as on the incisor surface. Hibernation in the common hamster, Cricetus cricetus, can be described as facultative with great individual variability of the body temperature dynamics during the winter. To investigate the records of hibernation on the incisor surface of this species, we studied the lower incisors of hamsters that had wintered with implanted temperature data loggers under natural conditions in a city park of Simferopol, Crimea (two animals); in semi-natural conditions in the village of Khunzakh, Dagestan (two animals); and using 19 hamsters from a natural population found dead in Simpferopol or its environs during late winter or early spring. Previous studies of eight hamsters that were kept under laboratory conditions and that had received tetracycline injections confirmed the daily formation of the increments on the incisor surface. This data allowed us to find the part of the incisor that could have been formed during hibernation in the hamsters with implanted loggers. In three of four of them, the typical pattern of daily increments was disrupted in the parts presumably formed during hibernation. The patterns of disruption varied in different animals, and it was impossible to interpret them as a record of hibernation. Those hamsters revealed no sequences of narrow and clearer increments characteristic of the records of hibernation on incisors. Such a sequence was seen on incisors of only one of 19 hamsters from the natural population. Consequently, no unambiguous record of the periods of hypothermia was found on the surface of incisors in the common hamster. According to the data published earlier, hibernation records on incisors were found in other hamsters of the subfamily Cricetinae (the genera Allocricetulus and Mesocricetus, in particular). A comparison of the dynamics of body temperature during hibernation in these hamsters and in the common hamster allow us to surmise that the formation of narrow increments can be determined in part by the depth and duration of hypothermia, but it mainly depends on the duration of normothermia and the feeding habits of animals during hibernation.

Intra- and interspecies variations in, and the mechanism of the formation of, a "hibernation zone" on the incisor surface are described in three groups of rodents differing in the mode of hibernation, i.e. marmots, ground squirrels, and hamsters. The growth of their incisors proceeds during hibernation. In marmots and ground squirrels that do not feed during hibernation, mechanical stress on incisors before, during, and after hibernation changes significantly. During hibernation, their incisors show the minimal growth and form a "hibernation zone" on the surface. There are two characters of the "hibernation zone" that are common for marmots and ground squirrels: very narrow increments and changes in the enamel-dentin junction. Interspecies variations in the patterns of "hibernation zone" may be attributed to differences in climate. In hamsters that can feed during hibernation, mechanical stress on the incisors during hibernation changes less significantly, the growth of their incisors is more notable, the enamel-dentin junction on the incisor surface does not change, and the "hibernation zone" can be noted only because the increments are more narrow and distinct than daily ones. Interspecies variations in the record of hibernation in hamsters can be significant, up to absent. Perhaps these differences are related not so much to climate as to the patterns of hibernation.

© 2020 г. Г. А. Клевезальa, *, Е. А. Зайцеваb, **, Д. В. Щепоткинa, *** , Н. Ю. Феоктистоваb, ****, М. М. Чунковc, *****, А. В. Суровb, ****** aИнститут биологии развития им. Н.К. Кольцова РАН, Москва 119991, Россия bИнститут проблем экологии и эволюции им. А.Н. Северцова РАН, Москва 119071, Россия cПрикаспийский институт биологических ресурсов ДНЦ РАН, Республика Дагестан, Махачкала 367000, Россия *e-mail: klevezal@bk.ru ** e-mail: zaycevaolena@gmail.com ***e-mail: dm_shchepotkin@mail.ru ****e-mail: feoktistovanyu@gmail.com *****e-mail: chunkov@mail.ru ******e-mail: surov@sevin.ru Поступила в редакцию 14.02.2019 г. После доработки 20.02.2019 г. Принята к публикации 28.03.2019 г.

Abstract—The lower incisors of ten hamsters from the Khunzakh region of Dagestan were studied. One hamster implanted with a temperature data logger successfully survived one winter in natural conditions, and its body temperature curve revealed 25 episodes of hypothermia with the body temperature dropping to 1–9°C, i.e., the period of hibernation. On the surface of the incisors, against a background of very indistinct increments, a zone with more distinct increments was observed. From the apical part of the zone to its basal part, the width of these increments decreased to very narrow, almost indistinguishable increments, and then increased. A comparison of the number of increments formed after this zone with the number of days the hamster survived after arousal from hibernation indicated that the zone was formed during hibernation. The pattern of variation in the increment width in the “zone of hibernation” corresponded to that observed in the episodes of normothermia during hibernation. A similar “zone of hibernation” was seen on the incisor surface in six of nine specimens caught in the field in June to early July. The date of their arousal was calculated from the number of increments corresponded to the date of arousal of the hamsters in this region, according to field observations. The pattern of the hibernation record on the incisors of these hamsters was mainly similar to that in the hamster with the temperature data logger and also demonstrated individual variations. Due to the poor contrast of increments on the incisor surface of these hamsters, it is difficult to use this record of hibernation for precise calculation of the data of arousal or for estimation of the duration of every episode of normothermia during hibernation. However, it is possible among the animals caught in spring to early summer to distinguish specimens aroused earlier or later using the position of the “zone of hibernation” on the incisor. It is also possible to estimate the relative duration of periods with short or long episodes of normothermia using the ratio of fragments with different widths of the increment in the “zone of hibernation.”

Investigation of the incisors of 17 rodent species from 11 genera revealed substantial interspecific and intraspecific variations in the pattern of the daily increment on the incisor surface. The morphology of daily increments is described in detail. Interspecific variations in the pattern are correlated with interspecific variations in the daily activity rhythms in rodents. Intraspecific (up to individual) traits can be attributed to intraspecific (up to individual) differences in daily activity. We can conclude that the daily activity of an individual determines the pattern of its incisor growth rhythm, not being a direct cause of daily increment formation. Thus, the pattern of the increment on the incisor surface can be considered as recording the rhythm of the daily activity of a rodent during the period of incisor renewal.

To evaluate how the course of irregular winter hibernation is recorded in the incisor teeth of Allocricetulus hamsters, an analysis was performed of the incisor surface in seven A. curtatus and two A. eversmanni hamsters and stained section of the incisors in one A. curtatus hamster. The animals were kept in cages at natural temperature and photoperiod. Five hamsters were implanted with a temperature data logger, and another five received tetracycline injections (5–20 days before death). In addition, the incisor surface was examined in eight A. curtatus and eight A. eversmanni hamsters trapped in the field. In hibernating hamsters, the duration of alternating periods of hypothermia (torpor bouts) and normothermia (arousals) and their ratio varied irregularly and randomly within and between individuals. Increments on the incisor surface were of two types: wide and poorly defined or narrow and distinct. The increments in hamsters trapped in the field were slightly more distinct than in experimental captive animals, and those in two hamsters that failed to hibernate were similarly wide and indistinct. In hibernating hamsters, wide increments proved to correspond to long periods of normothermia, while narrow increments were formed when torpor bouts alternated with short arousals. More distinct narrow increments formed when torpor bouts followed by short (no more than 1.5-days) arousals occurred in a series rather than singly. Although the number of narrow increments was approximately similar to that of short arousals, in was impossible to localize the record of each particular hypo/normothermia episode on the incisor surface. Dentin layers in stained preparations had no definite pattern and corresponded to these episodes no better than the increments on the incisor surface. In general, the narrow and distinct increments in a given Allocricetulus hamster is evidence that the animal did hibernate, and the number of such increments indicates the approximate minimum number of torpor bouts followed by arousals. The record of winter hibernation on the incisors of Allocricetulus hamsters has a pattern similar to that in Mesocricetus brandti (Batavia et al., 2013) but significantly differs from the pattern described in M. raddei (Klevezal et al., 2012).

The surface of incisors in nine specimens of Allocricetulus hamsters and stained sections of incisors in one of them were investigated to assess the possibility of recording the irregular hibernation on the incisors' surface. The hamsters were kept outdoors in captivity, termoregisters were implanted to five of them, and tetracycline was administrated to five of them 5-20 days before the death. Besides, incisors of 16 specimens from nature were studied. In the hibernated hamsters, the lengths of hypothermia periods and normothernia periods following them, as well as the relation of adjacent periods varied irregularly within and between specimens. Two kinds of increments were visible on the incisors' surface: wide indistinct increments and narrower distinct ones. In the specimens from nature, the increments were slightly clearer than those in the experimental ones. All the increments were wide and indistinct in two specimens that did not hibernate. In the hibernated hamsters, wide indistinct increments formed during normothernia and narrow ones formed when periods of hypothermia were followed by relatively short (not more than 1.5 days) periods of normothermia. The more distinct narrow increments were seen when relatively long series of such short normothermia periods, not separate ones, took place. The number of narrow increments roughly corresponded to the number of short periods of normothermia, but there was no possibility to locate a record of each concrete hypo/normothermia episode on the incisor surface. The dentin layers in the stained incisor sections corresponded to hypo/normothermia episodes not better than the increments on the surface. As a whole, the narrower and more distinct increments on the surface of incisors in the specimen of Allocricetulus are an evidence of its hibernation, and the number of such increments indicates the minimal number of hypo/normothermia episodes. The record of hibernation in incisors of Allocricetulus is similar to the record described in incisors of Mesocricetus brandti (Batavia et al., 2013) and quite different from the record in incisors of Mesocricetus raddei (Klevezal et al., 2012).

The lower incisors of 80 specimens of of 1–10 years old killed in spring in the highland of the Tien Shan Mountains were investigated. On the surface of all the incisors, regular daily increments and “hibernation zones” were revealed. The mean width of increments was used as an indicator of the incisor growth rate before hibernation. We found that the mean width did not depend on the sex of animals, locality, and incisor length, but depended on animal age. The increment width significantly decreased, and the number of the increments formed before hibernation significantly increased with age. This means that the growth rate of the incisors and the intensity of their attrition decrease with the animals’ age. The decrease in the incisor growth rate with age is a manifestation of the well-known decrease with age in the intensity of all growth processes in mammals. As a result of this decrease, in the majority of old marmots under study, zones of hibernation were revealed in the basal as well as in the apical parts of the incisor. The zone in the basal part formed during the latest hibernation and the zone in the apical part corresponded to the previous one. Thus, the incisor preserved the record of the entire year of animal life.

The lower incisors of 80 specimens of Marmota baibacina of 1–10 years old killed in spring in the highland of the Tien Shan Mountains were investigated. On the surface of all the incisors, regular daily increments and “hibernation zones” were revealed. The mean width of increments was used as an indicator of the incisor growth rate before hibernation. We found that the mean width did not depend on the sex of animals, locality, and incisor length, but depended on animal age. The increment width significantly decreased, and the number of the increments formed before hibernation significantly increased with age. This means that the growth rate of the incisors and the intensity of their attrition decrease with the animals’ age. The decrease in the incisor growth rate with age is a manifestation of the well-known decrease with age in the intensity of all growth processes in mammals. As a result of this decrease, in the majority of old marmots under study, zones of hibernation were revealed in the basal as well as in the apical parts of the incisor. The zone in the basal part formed during the latest hibernation and the zone in the apical part corresponded to the previous one. Thus, the incisor preserved the record of the entire year of animal life.