Skull-Based Method of Age Determination for the Brown Bear Ursus arctos Linnaeus, 1758

==Abstract==

Due to the lack of a proper technique for determining the ages of brown bears, a simple and straightforward method that is based on published data and our own observations is proposed. This method is based on the simultaneous use of the following different skull parameters to more accurately determine the ages of brown bears: size and weight parameters, degree of obliteration of the joints, degree of wear of the teeth, and development of the flanges. The proposed method contributes to non-destructive age determination, allows for the discrimination of immature and adult bears and also classifies the skulls of adult animals into one of the five selected age groups.

==Keywords==

Brown bear ; Ursus arctos ; Age determination ; Skull ; Teeth ; Craniometry

==Determining the Age of the Skull: Challenges and Approaches==

The determination of the exact age of an animal presents certain difficulties when working with morphological material. The inclusion of the animal in a particular analysis and the interpretation of the results depend on the accuracy of the determination. Incorrect definitions lead to errors in the analysis of the data and potentially to the presentation of incorrect hypotheses, particularly when working with large animals (for example, brown bears) that live long lives, during which their morphological characteristics change.

To solve this problem, it is necessary to create a methodology for determining the age of the studied species. Accounting for a greater number of parameters that change with age (such as size, weight and craniometrical indicators) increases the probability of at least identifying the age within a range of 2 to 3 years if not the specific age.

The parameters available for reviews also vary depending on the material that is being examined. For example, when working with live animals, craniometrical indicators are not available. The well-proven methods of age determination based on teeth cuts require destructive interference with the integrity of the skull, which is not always possible for work with museum specimens because it can lead to an inability to measure some of the parameters.

Our main goal was to evaluate the morphological diversity of the brown bear of Far East Russia. It is known that skull analyses often only use adults to exclude young, actively changing animals. However, according to various sources, brown bears can be considered to be adults and used for analysis purposes beginning at the age of 4–6 years ([[#bb0065|Krivocheev, 1984]] ). Therefore, the present study attempted to create a technique to determine the age of the brown bear based solely on the skull and to determine which age groups can be incorporated into this analysis.      

Prior to the age of three years, young bears do not exhibit any geographic variation in the structures of their skulls ([[#bb0070|Yudin et al., 1991]] ). Their skulls are characterized by a shortened and rounded brain cavity, quite narrow zygomatic arches and a direct transition from the forehead to the muzzle. At this age, the cranial sutures have not healed ([[#bb0060|Klevezal, 2007]] ). The full dental system is established by the age of approximately two years ([[#t0005|Table 1]] ; [[#bb0060|Klevezal, 2007]] ). After the third year, males exhibit more rugged features, that is, a high forehead, massive supraorbital spines, and wide cheekbones. The sexual characteristics are fully developed by the age of five years. Therefore, the skulls of bears younger than four years old cannot be used for morphological analysis.

<span id='t0005'></span>

{| class="wikitable" style="min-width: 60%;margin-left: auto; margin-right: auto;"
|+

Table 1.

Ages (months) of the appearances of the permanent teeth in the brown bear ''Ursus arctos''  according to different authors (see  [[#bb0060|Klevezal, 2007]] ).                  

|-

! colspan="7" | Tooth
! rowspan="2" | Entire dental system
! rowspan="2" | Source
|-

! i1, i2
! i3
! c
! p
! m1
! m2
! m3
|-

| 8
| 15
| 18
| 8
| 8
| 15
| 18
| 24 (?)
| [[#bb0095|Pearson, (1975)]]
|-

| 4–8
| 8–10
| 12
| 8–10
| 5
| 6–7
| 10–12
| 
| [[#bb0005|Adolf, (1949)]]
|-

| 5
| 8–10
| 12
| 6–8
| 
| 
| 10–12
| 
| [[#bb0010|Danilov et al. (1979)]]
|}

Due to the lack of an appropriate technique for determining the age of the brown bear, it was decided that a clear and simple methodology based on data from the literature ([[#bb0015|Zavatsky, 1977]] , [[#bb0020|Zavatsky, 1978]] , [[#bb0025|Zavatsky, 1981a]] , [[#bb0030|Zavatsky, 1981b]] , [[#bb0035|Zavatsky, 1984]] , [[#bb0040|Zavatsky, 1986a]] , [[#bb0045|Zavatsky, 1986b]] , [[#bb0050|Zavatsky, 1987]] , [[#bb0055|Zavatsky, 1991]] , [[#bb0070|Yudin, 1991]]  and [[#bb0060|Klevezal, 2007]] ) and proper research should be created. This methodology should meet a number of criteria. First, it cannot involve any destructive effects to the brown bears' skulls. Second, this methodology should utilize a sufficient number of parameters to reliably determine the age. Third, this methodology must be able to determine the age within a relatively narrow window, if not the exact age.      

Based on the use of the features that are directly related to the growth of the animal (e.g., the size of the skull), only the relative age can be determined and only a certain number of age groups can be highlighted, that is, growing animals during puberty. However, the skulls of some mammal species continue to grow after the age of sexual maturity ([[#bb0085|Gay and Best, 1996]] ). Moreover, the fact that individual differences in the sizes of mature individuals of the same age often exceed the skull size changes that occur with age should be noted ([[#bb0060|Klevezal, 2007]] ). Therefore, differences in the skull size can only be used as an additional parameter. The same limitation applies to the weight characteristics of the cranium. Moreover, several studies have utilized correlations between certain features rather than specific measurements to determine the age groups.      

Thus, for males below the age of 23 years, [[#bb0095|Pearson (1975)]]  elaborated the following equations for the relation between age (in years) and the zygomatic width of the skull (in mm) for two areas in the Yukon province in North America:
* lg (age) = 4,510008 ∗ lg (width) — 9.29264,
* lg (age) = 3,95651 ∗ lg (width) — 8.10864,

and for females in the 2 areas:
* lg (age) = 5,50499 * lg (width) — 11.39523.

For Balkan bears, the correlation between the age and the zygomatic width of the skull for males between the ages of 2 to 18 years is as follows ([[#bb0105|Sladek, 1992]] ):
* ln (age) = (width — 110.560): 37.186.

For females from 2 to 11 years of age, the following relation applies:
* ln (age) = (width — 123.916): 24.113.

Most often, age determination based only on the skull does not use the size and weight characteristics of the skull but rather uses the degree of obliteration of the joints and general changes in the shape of the surface of the skull. This method is appropriate for many mammalian species, but has most often been applied when dealing with carnivores, lagomorphs ([[#bb0075|Caboń-Raczyńska, 1964]] ) and rodents, which have teeth that grow constantly in yearly cubs ([[#bb0080|Daly, Patton, 1986]] ). Accordingly, this method functions well in determining the ages of yearling cubs. This method uses an indicator that changes with the size of the skull. The rapid growth of the length and width of the skull is only possible because the skull bones of young animals are not fused to one another and the skull sutures between the bones bond together with increasing size. The different sutures of the axial skull and mandible close up and disappear completely at different ages ([[#bb0060|Klevezal, 2007]] ). The conditions of several sutures allow for the discrimination of the ages of young animals when their dimensions are similar to those of adults and can also be used to discriminate younger adults from older animals ([[#bb0090|Lønø, 1970]] ). The development of the ridges is also used as a criterion for age definition. The skulls of young animals are smooth; however, with age, bumps and rough spots appear and develop into ridges (i.e., the arrow-shaped (or sagittal) and occipital ridges). The heights and lengths of the ridges increase with age. The development of ridges in females occurs later and is less extensive ([[#bb0060|Klevezal, 2007]] ).      

Another parameter used in the study of the age of mammals, particularly the brown bear, is the degree of tooth wear. When a tooth is completely cut and still non-functional, it has sharp enamel tips and bumps. Over the course of life and daily function, the tips slowly begin to fade. The enamel wears out completely, and there are outcrops of dentin that are a different colour. Furthermore, the bumps are ground, specific changes appear (e.g., the appearance of the trough in the middle row of the molars of the brown bear), the tooth surface flattens, and the height of the entire crown decreases ([[#bb0060|Klevezal, 2007]] ). Caries and hollows appear in the teeth of the oldest individuals.      

By accounting for a number of factors and parameters of the axial skull and mandible, the time interval of a brown bears age can be accurately specified, and yearling cubs, young pubescent and older individuals can be distinguished. Therefore, some parameters that may indicate age will be considered next. Controls for this type of research can be created by studying tooth slices, sections and skull bases of bears of precisely known ages, for example, bears from zoos and those under the supervision of researchers.

==Changes in the Parameters of the Skull with Age==

Young bears up to the age of four years will not be discussed in this review because morphological analyses are not applied to this age group. Notably, in the first three or four years of life, all of the molars in both jaws of cubs appear, the semicircular lines converge 3–4 cm from the occipital bone, the sagittal crest begins to grow, the squamous suture nearly closes, and the coronal suture begins to ankylose. The length of the sagittal crest of the male brown bear typically increases with age, but this phenomenon is less typical in females ([[#bb0060|Klevezal, 2007]] ).      

From the age of four, the lambdoidal, interfrontal, naso-maxillary, palato-maxillary and palatal sutures and suture between the maxillary and zygomatic bones begin to coalesce. The interfrontal suture is fully or partially closed in half of five-year old males and in 100% of males by the age of 14 years. This suture is closed in 80% of female individuals by the age of five years, and by the seventh year, it is closed in all females. The nasal suture begins to accrete in males by the age of six years and beyond. At approximately the same time, that is, the age of 6 to 11 years, the coronal and frontal sutures are in the process of accretion (or are already closed). By the age of 6 to 8 years, the sagittal crest begins to extend beyond the coronal suture in males, but can occasionally remain short at later ages ([[#bb0105|Sladek, 1992]] ). The beginning of the coalescence of the nasal suture is observed in females by the age of 5 years, and complete coalescence is achieved in 14-year-old females ([[#bb0060|Klevezal, 2007]] ). By the age of approximately 7 to 10 years, the frontomaxillary suture closes, but may remain in the accretion stage until the age of 12 to 14 years. By 12 to 14 years, the palato-maxillary and intermaxillary sutures are completely closed and the palatal suture completely accretes in the middle. The average age of males with closed nasal and naso-frontal sutures is not less than 12 years, and this age for females is not less than 10 years ([[#bb0095|Pearson, 1975]] ). By the age of 15 to 18 years, all cranial sutures have completely coalesced. Only the seams between the zygomatic bone and the mandible remain ununited. These seams coalesce only after 18 years ([[#bb0020|Zavatsky, 1978]]  and [[#bb0105|Sládek, 1992]] ).      

Based on the tooth system, some age estimates for brown bears can also be given. For example, the rear edges of the upper incisors begin to be ground down by approximately 4 to 6 years of age. In their fourth summer, some individuals exhibit the first traces of ground canines. The apical foramen of the roots of the canines closes during the 5th or 6th summer ([[#bb0100|Rausch, 1969]] ). Later, by the age of 6 years, the end maxillary incisors become 5–6 mm higher than the middle teeth. By the ages of 8 to 9 years in males and 6 to 7 years in females, M3 begins to be ground down ([[#bb0105|Sládek, 1992]] ). At this age, the tuberosity of molar row is still clearly visible, and all tip sections of the carnassials are sharp. Closer to 12 to 14 years, the internal vertex predatory teeth begin to grind. A canal appears in the middle of the molars. The end incisors are ground to nearly the mid-tooth level. By the age of 15 to 18 years, brown bears have worn down the external vertexes of the predatory upper teeth and pits have formed on the inner side. The canal of the upper molar row deepens. The end incisors of both jaws wear down to the level of the cardinal teeth. Among bears over 18 years old, most of the molars typically have caries and the upper molars have hollows. The upper molar row is ground on the inner side and in the middle. Its outer edge becomes sharp and is 8–10 mm above the internal edge. Some teeth may be missing, and the canines are often broken.      

Because individual variability is very high, it is impossible to define the exact age of a brown bear based only on the cranial and dental characteristics, even if large numbers of such characteristics are used. Therefore, we propose a scheme in which several age groups of bears are identified. Each group has distinctive properties. In total, we identified the following five groups: 4–6 years, 6–11 years, 12–14 years, 15–18 years, and over 18 years. The group with the widest variation was found to be the 6–11-year group because the animal experiences many changes at this age; however, it did not appear to be possible to break this group down in additional subgroups. Over the course of this work, a scheme ([[#t0010|Table 2]] ) was created by combining all of the available data from different authors ([[#t0010|Table 2]] ). This scheme should simplify the procedure of age determination for both male and female brown bears.

<span id='t0010'></span>

{| class="wikitable" style="min-width: 60%;margin-left: auto; margin-right: auto;"
|+

Table 2.

Correspondences of axial skull and mandible parameters with age in brown bears.

|-

! rowspan="2" | Characteristics
! colspan="6" | Age groups
|-

! Less than 3 years old
! 4–6 years old
! 6–11 years old
! 12–14 years old
! 15–18 years old
! 18 or more years old
|-

| Basal length, mm
| 150–285
| 283–304
| 295–323
| 323–347
| 333–371
| 
|-

| Weight of brain pan, gr.
| 80–610
| 560–870
| 700–1100
| 1100–1340
| 1130–1500
| 
|-

| Length of sagittal crest, cm
| 
| > 3
| 9–11
| 
| 
| 
|-

| Height of sagittal crest, cm
| 
| 0,5
| 1,5–2
| 2,5–2,7
| 
| 
|-

| Squamous suture
| Almost coalesced
| +/−
| Coalesced
| Coalesced
| Coalesced
| Coalesced
|-

| Coronal suture
| Starts to coalesce
| +/−
| Coalesced
| Coalesced
| Coalesced
| Coalesced
|-

| Suture between maxillary and zygomatic bones
| −
| Starts to coalesce
| +/−
| Coalesced
| Coalesced
| Coalesced
|-

| Nasal suture
| −
| −
| Coalesced
| Coalesced
| Coalesced
| Coalesced
|-

| Frontal suture
| −
| −
| In the process of coalescence (or already coalesced)
| Coalesced
| Coalesced
| Coalesced
|-

| Palatomaxillary suture
| −
| −
| −
| Coalesced
| Coalesced
| Coalesced
|-

| Palatine suture
| −
| −
| −
| Coalesced in the middle
| Coalesced
| Coalesced
|-

| Intermandibular suture
| −
| −
| −
| Coalescing
| Coalesced
| Coalesced
|-

| Suture between supramaxillary and frontal bones
| −
| −
| −
| In the process of coalescence
| Coalesced
| Coalesced
|-

| Mandible bones and jugal bridge remain in the process of coalescence
| −
| −
| −
| −
| +
| +
|-

| Jugal bridge coalesced
| −
| −
| −
| −
| −
| +
|-

| Mandible bones coalesced
| −
| −
| −
| −
| −
| +
|-

| Apical aperture of canine radix is closed
| −
| + (5–6 years)
| +
| +
| +
| +
|-

| Rear edge of upper incisors
| 
| Is ground
| 
| 
| 
| 
|-

| Central incisors
| 
| 
| Ground evenly
| 
| 
| 
|-

| End incisors
| 
| 
| Ground from the inner side
| Ground to the level of cardinal teeth
| 
| 
|-

| End incisors of maxilla
| 
| 
| 5–6 mm higher than the cardinal teeth
| 
| 
| 
|-

| End incisors of both jaws
| 
| 
| 
| 
| Worn to the level of cardinal teeth
| 
|-

| М3 starts to grind
| −
| −
| + (at age of 8–9 years of males and 6–7 years of females)
| 
| 
| 
|-

| Tuberosity of molar row is still easy to see
| +
| +
| +
| −
| −
| −
|-

| All vertex of predatory teeth are sharp
| +
| +
| +
| −
| −
| −
|-

| Inner edges of molars have ground 2–5 mm more than the outer ones
| −
| −
| +
| 
| 
| 
|-

| Inner vertex of predatory tooth has ground
| −
| −
| −
| +
| 
| 
|-

| Canal has appeared in the middle of molar row
| −
| −
| −
| +
| 
| 
|-

| External vertexes of predatory teeth have ground, on the inner side there is hole
| −
| −
| −
| −
| +
| 
|}

Note: “+” indicates that the characteristic is present, “−” indicates that the characteristic is absent, and “+/−” indicates that the characteristic may be present but not in all individuals (due to the wide individual variability).

[[#t0010|Table 2]]  shows that immature bears can be distinguished from adult animals based on the skull and also demonstrates the features of brown bear development during the postnatal period. The proposed method also contributes to the non-destructive determination of age. However, according to [[#bb0095|Pearson (1975)]] , the usage of the degree of suture obliteration as a criterion for age determination is limited by the sufficiently large individual variability. For this reason, this method is inferior in accuracy to other methods, for example, determinations of age based on epiphysis ossification or slices and sections of the teeth.      

This technique will be improved. This technique requires a large amount of material that can be collected through the cooperation of many researchers and hunting management personnel.

==References==

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</ol>