Cementum Age Determination for Grizzly Bears in the Greater Yellowstone Ecosystem
Photo: A grizzly bear crosses the Moose-Wilson Road in Grand Teton National Park. This is likely grizzly 760. Photo credit: USFWS/NPS
When grizzly bears are captured in the Greater Yellowstone, a tooth will be extracted for aging purposes (if the bear is recaptured, no tooth is taken). The method used to age bears is referred to as cementum aging, which requires extracting a molar (PM1) and examining the cementum layers microscopically. The annuli, formed by the cementum, can be counted for numerous species, and there is a positive correlation between cementum rings and animal age. Cementum annuli are considered the most reliable indicators of age, respectively, for black bears (Marks and Erickson, 1966; Stoneberg and Jonkel, 1966; Hildebrandt, 1976; Rogers, 1978; Matson's Lab, 1988) and numerous (40+) mammalian species (Thomas, 1977). The oldest bears documented using this procedure in the Greater Yellowstone Ecosystem (GYE) are listed below:
The first efforts to use growth layers in teeth for aging purposes was conducted by Scheffer (1950) & Laws (1952, 1953). Mundy & Fuller (1964) were among the first to employ cementum layering in M3 to calculate grizzly bears' age. While they did lack known age specimens, they discovered a positive correlation between the number of annuli present and the zygomatic breadth. They believed that one annulus is created per year in the cementum; however, they did not yet understand the layering process.
The first efforts to use growth layers in teeth for aging purposes was conducted by Scheffer (1950) & Laws (1952, 1953). Mundy & Fuller (1964) were among the first to employ cementum layering in M3 to calculate grizzly bears' age. While they did lack known age specimens, they discovered a positive correlation between the number of annuli present and the zygomatic breadth. They believed that one annulus is created per year in the cementum; however, they did not yet understand the layering process.
Terms and Important Definitions:
Annulus = the annual dark cementum layer(s) in a tooth. It can be simple with a single component or can be complex with more than one component.
Annuli = referred to in the literature as layers, rings, bands; minor components = false annuli.
Light cementum = abundant, cellular cementum lightly stained in histological sections viewed with transmitted light. Produced during spring and summer in the northern hemisphere
Dark cementum = acellular cementum darkly stained in histological sections viewed with transmitted light. Produced during winter in the northern hemisphere; produced during other seasons resulting in complex annual layers of light and dark cementum.
Annulus = the annual dark cementum layer(s) in a tooth. It can be simple with a single component or can be complex with more than one component.
Annuli = referred to in the literature as layers, rings, bands; minor components = false annuli.
Light cementum = abundant, cellular cementum lightly stained in histological sections viewed with transmitted light. Produced during spring and summer in the northern hemisphere
Dark cementum = acellular cementum darkly stained in histological sections viewed with transmitted light. Produced during winter in the northern hemisphere; produced during other seasons resulting in complex annual layers of light and dark cementum.
Figure: Dental diagram of the structure of the first premolar.
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Figure: Diagram pointing out the location of the upper first premolar in a bear skull (this is the preferred tooth to sample for annular cementum aging in black, grizzly and brown bears).
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Why the first premolar?
The Upper Premolar Number 1 (UPM1) is typically favored for sectioning because it is nearly straight and has a rounded tip. The Lower Premolar Number 1 (LPM1) is more challenging to section in the longitudinal plane due to it being curved and having a pointed tip. The upper PM1 has been selected as a standardized tooth for four reasons (Matson et al. 1993):
1.) Its small size enables convenience for processing;
2.) the tooth may be extracted from live bears;
3.) the natural shape of the tooth allows for more reliable sectioning (less curved and less pointed than lower PM1
4.) eruption occurs early in life; the annulus is present the first winter. Frankly, it is favorable to use only this specific tooth type for annular cementum aging to reduce annuli characteristics variation.
The Upper Premolar Number 1 (UPM1) is typically favored for sectioning because it is nearly straight and has a rounded tip. The Lower Premolar Number 1 (LPM1) is more challenging to section in the longitudinal plane due to it being curved and having a pointed tip. The upper PM1 has been selected as a standardized tooth for four reasons (Matson et al. 1993):
1.) Its small size enables convenience for processing;
2.) the tooth may be extracted from live bears;
3.) the natural shape of the tooth allows for more reliable sectioning (less curved and less pointed than lower PM1
4.) eruption occurs early in life; the annulus is present the first winter. Frankly, it is favorable to use only this specific tooth type for annular cementum aging to reduce annuli characteristics variation.
The aging method can be referred to as the Cementum Aging Model for brown bears (applicable for black, grizzly, and brown bears).
Provides consistent determination of cementum ages by:
1.) Reporting characteristics of first premolar (PM1) in detail, which includes the most probable sources of error
2.) Normalizing the criteria for PM1 cementum aging
3.) Using pictures and photographs of known age tooth sections as training tools
4.) Outlining and defining the steps in tooth processing and section preparation that require standardization
Provides consistent determination of cementum ages by:
1.) Reporting characteristics of first premolar (PM1) in detail, which includes the most probable sources of error
2.) Normalizing the criteria for PM1 cementum aging
3.) Using pictures and photographs of known age tooth sections as training tools
4.) Outlining and defining the steps in tooth processing and section preparation that require standardization
Figure: Comparison of ages derived from the lower, fourth premolar tooth sections of young grizzly bears in Yellowstone National Park.
Histology of tooth sections:
Tooth and dental histology, along with the interpretation of structures used in annular cementum aging, have been reviewed in detail (Klevezal & Kleinenberg, 1969; Johnston et al., 1987).
The typical first premolar mid-sagittal section: the eruption of permanent premolar teeth typically occurs before the northern interior grizzlies den (Pearson, 1975). Additionally, Mundy and Fuller (1964) and Stoneberg and Jonkel (1966) gathered that the 'dark line' is being produced before grizzly bears or black bears enter their dens.
In spring, the first premolar of a yearling bear will have light cementum from the previous summer/fall and one annulus from the prior winter. Identifying the first annulus is obtained from the correct identification of the dentine-cementum junction (PHOTO). The dentine-cementum junction is described as the border between the striated dentine and "spongy" cementum. Both dentine and cementum are developed throughout a bear's life. Dentine is produced by cells lining the pulp cavity; this inevitably reduces the size of the cavity. Cementum production occurs when cells on the outer surface of the tooth's root steadily grow the root's diameter (Matson et al. 1993).
The periodontal membrane serves as a crucial indicator that all cementum is present at the point when observed. It is possible to remove cementum accidentally if improper tooth extraction and lab processing techniques are employed (Matson et al. 1993). Past research also presumed that cementoblast cells of the periodontal membrane are active in grizzly bears from 6 months to 14.5 years old (Craighead & Craighead, 1970)
Thin annual light cementum layers have been correlated with successful cub rearing in adult female black bears (Carrel 1992; Coy & Garshelis, 1992). It is unexplained whether the same layers can be reliably identified in the cementum of female brown bears.
Additionally, the cementum layers tend to diminish in thickness with age, meaning in older bears, the annuli becomes increasingly challenging to count (Craighead & Craighead, 1970). Constricted and sometimes uneven layering in older or geriatric bears' outer growth layers makes it complicated to assign an age closer than +/- 1 year.
Tooth and dental histology, along with the interpretation of structures used in annular cementum aging, have been reviewed in detail (Klevezal & Kleinenberg, 1969; Johnston et al., 1987).
The typical first premolar mid-sagittal section: the eruption of permanent premolar teeth typically occurs before the northern interior grizzlies den (Pearson, 1975). Additionally, Mundy and Fuller (1964) and Stoneberg and Jonkel (1966) gathered that the 'dark line' is being produced before grizzly bears or black bears enter their dens.
In spring, the first premolar of a yearling bear will have light cementum from the previous summer/fall and one annulus from the prior winter. Identifying the first annulus is obtained from the correct identification of the dentine-cementum junction (PHOTO). The dentine-cementum junction is described as the border between the striated dentine and "spongy" cementum. Both dentine and cementum are developed throughout a bear's life. Dentine is produced by cells lining the pulp cavity; this inevitably reduces the size of the cavity. Cementum production occurs when cells on the outer surface of the tooth's root steadily grow the root's diameter (Matson et al. 1993).
The periodontal membrane serves as a crucial indicator that all cementum is present at the point when observed. It is possible to remove cementum accidentally if improper tooth extraction and lab processing techniques are employed (Matson et al. 1993). Past research also presumed that cementoblast cells of the periodontal membrane are active in grizzly bears from 6 months to 14.5 years old (Craighead & Craighead, 1970)
Thin annual light cementum layers have been correlated with successful cub rearing in adult female black bears (Carrel 1992; Coy & Garshelis, 1992). It is unexplained whether the same layers can be reliably identified in the cementum of female brown bears.
Additionally, the cementum layers tend to diminish in thickness with age, meaning in older bears, the annuli becomes increasingly challenging to count (Craighead & Craighead, 1970). Constricted and sometimes uneven layering in older or geriatric bears' outer growth layers makes it complicated to assign an age closer than +/- 1 year.
Photo: The D/C represents the dentine-cementum junction referenced in the text.
Standardized method for annular cementum aging (longitudinal sections) upper & lower premolars (PM1 & PM3):
Annular cementum aging error may be lessened and decreased by reporting sources of error in detail while concurrently establishing specific criteria that allow the ager to recognize them during the aging process (Matson et al. 1993)
1.) Ensure to look at the collection date for the tooth. The last formed annulus from teeth collected during the spring will be too close to the root's outer surface, sometimes making it not apparent without cautious and thorough observation.
2.) Examine and scan the complete sampled section at low magnification for points where annuli are the most profound
3.) Count annuli of at least two points within the same section, and do this for at least two sections
a. Meticulously observe the dentine-cementum junction with critical attention to the 1-year growth layer; analyze the junction closely at all points within the section.
b. Counts will have to be performed while moving the section due to the early and late annuli being prominently visible at different points within the section. What does this mean? A single point within the section may not visibly show cementum layers of both early and later years.
4.) Investigate and resolve differences in the count by re-examining, expressly with particular attention to the criteria for the 1-year layer and complex layer groups
5.) Review and observe all points of the section for evidence that does not verify the determined age. If any evidence is identified, begin again with the age determination of the section
6.) Designate a reliability index to the determined age
Annular cementum aging error may be lessened and decreased by reporting sources of error in detail while concurrently establishing specific criteria that allow the ager to recognize them during the aging process (Matson et al. 1993)
1.) Ensure to look at the collection date for the tooth. The last formed annulus from teeth collected during the spring will be too close to the root's outer surface, sometimes making it not apparent without cautious and thorough observation.
2.) Examine and scan the complete sampled section at low magnification for points where annuli are the most profound
3.) Count annuli of at least two points within the same section, and do this for at least two sections
a. Meticulously observe the dentine-cementum junction with critical attention to the 1-year growth layer; analyze the junction closely at all points within the section.
b. Counts will have to be performed while moving the section due to the early and late annuli being prominently visible at different points within the section. What does this mean? A single point within the section may not visibly show cementum layers of both early and later years.
4.) Investigate and resolve differences in the count by re-examining, expressly with particular attention to the criteria for the 1-year layer and complex layer groups
5.) Review and observe all points of the section for evidence that does not verify the determined age. If any evidence is identified, begin again with the age determination of the section
6.) Designate a reliability index to the determined age
Variation and Sources of Error in Annular Cementum Age Determination
Interestingly, one study (McLaughlin et al. 1990) determined that experienced readers (agers) assigned significantly lower age estimates than inexperienced readers (agers) in both young and old age bears; the most remarkable differences were documented in older bears. The precision with age estimation does exhibit variation within and among readers depending on their experience levels (McLaughlin et al. 1990). This remains consistent with previously published data that the cementum layers tend to decrease in thickness with age, meaning in older bears, the annuli become increasingly challenging to count (Craighead & Craighead, 1970). For an inexperienced ager, this could be an impediment. Most readers and agers learn the process and methodology of age estimation by cementum annuli through tutoring by an experienced reader or ager, not through reading large numbers of slides from known-age bears. Furthermore, age estimates insinuate that experienced agers use more robust criteria for identifying annuli than inexperienced agers (McLaughlin et al. 1990).
The five most common sources of error in annular cementum aging techniques are listed below. For more in-depth information on these sources of error, refer to Matson et al. 1993.
1.) Last-formed annulus misinterpretation in spring collected teeth
2.) The variable distance of the 1-year annulus from the dentine-cementum junction
3.) Complex annuli
4.) Portions of the tooth abnormal, damaged or missing
5.) Indistinct annuli
Interestingly, one study (McLaughlin et al. 1990) determined that experienced readers (agers) assigned significantly lower age estimates than inexperienced readers (agers) in both young and old age bears; the most remarkable differences were documented in older bears. The precision with age estimation does exhibit variation within and among readers depending on their experience levels (McLaughlin et al. 1990). This remains consistent with previously published data that the cementum layers tend to decrease in thickness with age, meaning in older bears, the annuli become increasingly challenging to count (Craighead & Craighead, 1970). For an inexperienced ager, this could be an impediment. Most readers and agers learn the process and methodology of age estimation by cementum annuli through tutoring by an experienced reader or ager, not through reading large numbers of slides from known-age bears. Furthermore, age estimates insinuate that experienced agers use more robust criteria for identifying annuli than inexperienced agers (McLaughlin et al. 1990).
The five most common sources of error in annular cementum aging techniques are listed below. For more in-depth information on these sources of error, refer to Matson et al. 1993.
1.) Last-formed annulus misinterpretation in spring collected teeth
2.) The variable distance of the 1-year annulus from the dentine-cementum junction
3.) Complex annuli
4.) Portions of the tooth abnormal, damaged or missing
5.) Indistinct annuli
Reliability Index for Annular Cementum Aging:
The ager should declare varying degrees of confidence among samples by specifying each a reliability index. It is imperative to note the index is a subjective judgment of accuracy. The consequences of error for younger bears are more significant, so similarly, the precision required for the highest reliability rating is greater.
Whenever the individual aging feels or resolves that their findings and results may not be accurate, the range of possible results should be given (accompanied by a specified range of possible ages). The age which is described as the primary result should be the one supported by the most reliable available evidence (Matson et al. 1993)
The ager should declare varying degrees of confidence among samples by specifying each a reliability index. It is imperative to note the index is a subjective judgment of accuracy. The consequences of error for younger bears are more significant, so similarly, the precision required for the highest reliability rating is greater.
Whenever the individual aging feels or resolves that their findings and results may not be accurate, the range of possible results should be given (accompanied by a specified range of possible ages). The age which is described as the primary result should be the one supported by the most reliable available evidence (Matson et al. 1993)
Figure: This tooth was extracted from a female black bear wih a known age of 4 years and was incorrectly aged as 2 years old. The 2 distinct annuli, and intact cementum layer as evidenced by the presence of the periodontal membrane suggests this aging error is the result of tooth misidentification.
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Figure: This tooth was extracted from a 9 year-old known age female black bear, who was aged incorrectly as 7 years-old. Nine annuli might have been visible if the tooth had not been broken. In addition, the crown of the tooth was removed below the gum line, which may have created further difficulty in age estimation. Tooth breakage during extraction and poor tooth preparation are important sources of error when aging teeth.
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Tooth Extraction:
The following steps listed below are the published standardized procedures for tooth extraction in bears (Matson et al. 1993):
1.) Position the bear's head with easy access to the tooth, where leverage is sufficient for pulling. The jaw of the bear should be opened wide. If the bear is alive and anesthetized, place a block between the upper and lower molars
2.) Lightly push the tooth elevator between the tooth and the gum at an angle that is parallel to the long axis of the tooth. Slide the elevator around the tooth and make sure to apply enough pressure to extricate the tooth. Do not use the elevator to pry the tooth from the jaw. Be sure and cautious not to gouge or scratch the tooth while employing the elevator.
3.) Grab the crown of the tooth securely with a dental extractor and make a strong pull in line with the long axis of the tooth; pull the tooth straight out of the socket
4.) Place the extracted tooth in a paper envelope and appropriately label (tooth type, species, sex of the bear, date of kill or tooth extraction, location, and any other relevant info)
5.) Teeth should stay in their envelope and stored in a dry and cool place until they are sent off to the lab for examination; teeth can be frozen if they need to be stored for more than several weeks.
The following steps listed below are the published standardized procedures for tooth extraction in bears (Matson et al. 1993):
1.) Position the bear's head with easy access to the tooth, where leverage is sufficient for pulling. The jaw of the bear should be opened wide. If the bear is alive and anesthetized, place a block between the upper and lower molars
2.) Lightly push the tooth elevator between the tooth and the gum at an angle that is parallel to the long axis of the tooth. Slide the elevator around the tooth and make sure to apply enough pressure to extricate the tooth. Do not use the elevator to pry the tooth from the jaw. Be sure and cautious not to gouge or scratch the tooth while employing the elevator.
3.) Grab the crown of the tooth securely with a dental extractor and make a strong pull in line with the long axis of the tooth; pull the tooth straight out of the socket
4.) Place the extracted tooth in a paper envelope and appropriately label (tooth type, species, sex of the bear, date of kill or tooth extraction, location, and any other relevant info)
5.) Teeth should stay in their envelope and stored in a dry and cool place until they are sent off to the lab for examination; teeth can be frozen if they need to be stored for more than several weeks.
Estimating age based on tooth wear
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During capture and immobilization procedures, it use to be conventional for researchers and scientists to extract a tooth to age a bear. The most reliable method to age a bear is by extracting a molar (PM1) and examining the cementum layers microscopically. However, extracting a tooth is not always practical nor favored by many wildlife professionals. Immobilization and capture already infer a certain level of invasive procedures, and during such activity, it is vital to minimize needless invasive and otherwise stressful procedures at the bear's expense. In the field, researchers and wildlife professionals can approximate and estimate a bear's age by examining the physical state of their dentition (Palmisciano 1988, LeCount 1986).
There are, however, downfalls to this method because of the variability of tooth wear, generally related to diet. Grizzly bears show remarkable plasticity in their diets. It is theorized that bears residing in habitats with dry and rocky regions, where roots and tubers are eaten, that teeth can receive more notable wear because of the abrasive nature of soils. Also, it has been noticed that bears that reside and are handled in heavily managed ecosystems (Yellowstone, Glacier, etc.) have a higher incidence of broken or damaged teeth (Jonkel 1993). Some of these can be associated with damage caused during trapping operations with culvert traps, while some may be attributed to natural processes of "wear and tear" on the dentition.
There are, however, downfalls to this method because of the variability of tooth wear, generally related to diet. Grizzly bears show remarkable plasticity in their diets. It is theorized that bears residing in habitats with dry and rocky regions, where roots and tubers are eaten, that teeth can receive more notable wear because of the abrasive nature of soils. Also, it has been noticed that bears that reside and are handled in heavily managed ecosystems (Yellowstone, Glacier, etc.) have a higher incidence of broken or damaged teeth (Jonkel 1993). Some of these can be associated with damage caused during trapping operations with culvert traps, while some may be attributed to natural processes of "wear and tear" on the dentition.
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If there is ever any skepticism about the species being handled, you can measure the length of the last upper molar (M2). Black bears have an M2 that is < 1 1/8 inches in length; grizzlies have M2 that are > than 1 1/8 inches in length.
A bear's size can be misleading, especially during the fall when hyperphagia is in full swing. While size may be misleading and allow an individual to confuse a cub or yearling to a subadult, distinct dentition provides a more definitive answer. Listed are dental criteria based upon bear age (Palmisciano 1988):
Cub (during spring)
When examining dentition after a bear's first year, it is imperative to note and observe the canines and incisors' condition and color. Over time, permanent teeth will change color and yellow, or turn brown; they will wear flat or begin to round, crack/split, sometimes even breaking entirely off.
2-4 year-olds
Bears that are 15 years old and older, especially males, are generally quite large and surprisingly healthy. The oldest bear captured was 32 years old, in the Cabinet Mountains (Kasworm & Manley 1988). The bear's teeth were broken, and its incisors were worn down to the right above the gum line; however, the bear's general body assessment and condition were still fair. Senior bears (15+) may have more difficulty biting, shearing, and grinding up food than younger bears, which may be compensated by a senior bear's experience and efficiency when finding and locating a food source. Ultimately, the natural life of bears depends on their dental health (Jonkel 1993)
A bear's size can be misleading, especially during the fall when hyperphagia is in full swing. While size may be misleading and allow an individual to confuse a cub or yearling to a subadult, distinct dentition provides a more definitive answer. Listed are dental criteria based upon bear age (Palmisciano 1988):
Cub (during spring)
- Deciduous teeth, various stages of eruption
- Molars not yet present
- Middle permanent incisors (I1) starting to erupt (maybe)
- Canines deciduous
- Molar 1 and incisor 1 nearly erupted
- Incisor 2 tips visible in gums
- Cub (during fall)
- Canines are deciduous, just starting to erupt
- Molars 1 & 2, plus all incisors, are mostly erupted
- Molar 3 on the lower jaw will be absent, or barely even visible
- Will have all permanent teeth
- Canines and 3rd molar = partially erupted
- Best gauge = canine, which will be 1/8 to ½ erupted
- Yearling (during mid-summer)
- Lower 3rd molar = mostly grown
- Canine = ½ to ¾ erupted
- Teeth appear smooth, unworn
- Canine = 7/8 erupted
When examining dentition after a bear's first year, it is imperative to note and observe the canines and incisors' condition and color. Over time, permanent teeth will change color and yellow, or turn brown; they will wear flat or begin to round, crack/split, sometimes even breaking entirely off.
2-4 year-olds
- Smooth, white teeth
- Canine tips, incisors square off; cusps visible
- Canines flattened tips
- Incisors are worn flat
- Middle incisors = cusps still present with dentine spots
- Most teeth stained yellow
- Canines flattened and yellow, some hairline cracks
- All incisors are worn flat
- Two lower incisors show more wear
- Canines discolored, flattened (cracked or broken)
- Incisors visible barely above the gum line; worn straight across
- Two lower middle incisors, worn, slightly rounded (maybe broken)
- Excessively worn & discolored, broken front teeth
- Molars intact, slight wear, heavily stained dark yellow, brown hues
- Canines may be broken or rounded smooth at the gum line
- The remaining canines split/splintered, cracked, broken
- All incisors are usually worn straight across at gum line
- Lower incisors have rounded crowns
Bears that are 15 years old and older, especially males, are generally quite large and surprisingly healthy. The oldest bear captured was 32 years old, in the Cabinet Mountains (Kasworm & Manley 1988). The bear's teeth were broken, and its incisors were worn down to the right above the gum line; however, the bear's general body assessment and condition were still fair. Senior bears (15+) may have more difficulty biting, shearing, and grinding up food than younger bears, which may be compensated by a senior bear's experience and efficiency when finding and locating a food source. Ultimately, the natural life of bears depends on their dental health (Jonkel 1993)
Photo: Young grizzly bear displaying its teeth as it bites into a log. Notice the yellow staining of the teeth.
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Photo: Notice the differences in the physical appearance of a male grizzly bear (bottom) versus a female grizzly bear (top). Color variation, breadth of the head (zygomatic arches) and body size. However, sometimes size and color are poor and inconsistent indicators of sex. Photo courtesy of Kerry Gunther/NPS (bottom) and Yellowstone National Park/NPS (top)
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Identifying sex based on physical characteristics:
As a general rule of thumb, females and subadult grizzly bears generally tend to be lighter in color than adult male bears (Jonkel 1993). Male grizzly bears have a "blocky" appearance, with wider noses, giant heads, and bodies than females. A parallel could be drawn to female and male Labrador retrievers; males have blocky heads and typically have larger bodies.
As a general rule of thumb, females and subadult grizzly bears generally tend to be lighter in color than adult male bears (Jonkel 1993). Male grizzly bears have a "blocky" appearance, with wider noses, giant heads, and bodies than females. A parallel could be drawn to female and male Labrador retrievers; males have blocky heads and typically have larger bodies.
Figure: Weights documented by age class between spring and fall for female grizzly bears. Data compiled and used to create this chart was obtained via Blanchard 1986, and later published again in Jonkel 1993.
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Figure: Weights documented by age class between spring and fall for male grizzly bears. Data compiled and used to create this chart was obtained via Blanchard 1986, and later published again in Jonkel 1993.
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Works Cited
[1.] Blanchard , B. M. (1986). Yellowstone grizzly size/growth patterns. International Conference of Bear Research and Management. 7:21-25
[2.] Carrel, W. K. (1992). Reproductive history in dental cementum of female black bears. In International Conference on Bear Research and Management (Vol. 9, No. 1, pp. 205-12).
[3.] Coy, P. L., & Garshelis, D. L. (1992). Reconstructing reproductive histories of black bears from the incremental layering in dental cementum. Canadian Journal of Zoology, 70(11), 2150-2160.
[4.] Craighead, J. J., Craighead Jr, F. C., & McCutchen, H. E. (1970). Age determination of grizzly bears from fourth premolar tooth sections. The Journal of Wildlife Management, 353-363.
[5.] Elbroch, M. (2006). Animal skulls: a guide to North American species. Stackpole Books.
[6.] Hildebrandt, T.D. 1976. Age determination in Michigan black bear by means of cementum annuli. Mich. Dep. Nat. Resour. Rep. No. 2758., Lansing.
[7.] Johnston, D. H., Joachim, D. G., Bachmann, P., Kardong, K. V., Stewart, R. E. A., Dix, L. M., ... & Watt, I. D. (1987). Aging furbearers using tooth structure and biomarkers. Nowak, M.; Baker, JA; Obbard, ME, 228-243.
[8.] Jonkel, J. L. (1993). A manual for handling bears for managers and researchers. US Fish and Wildlife Service, Office of Grizzly Bear Recovery.
[9.] Kasworm, W., & Manley, T. L. (1988). Grizzly bear and black bear ecology in the Cabinet Mountains of northwest Montana. The Department.
[10.] Klevezalʹ, G. A., & Kleinenberg, S. E. E. (1969). Age determination of mammals from annual layers in teeth and bones.
[11.] Laws, R. M. (1952). A new method of age determination for mammals. Nature, 169(4310), 972-973.
[12.] Laws, R. M. (1953). A new method of age determination in mammals with special reference to the elephant seal (Mirounga leonina, Linn.).
[13.] LeCount, A. L. (1986). Black bear field guide: a manager's manual (No. 16). Research Branch, Arizona Game and Fish Department.
[14.] Marks, S. A., & Erickson, A. W. (1966). Age determination in the black bear. The Journal of Wildlife Management, 389-410.
[15.] Matson, G. M. L. J., Van Daele, L., Goodwin, E., Aumiller, L., Reynolds, H., & Hristienko, H. (1993). A laboratory manual for cementum age determination of Alaska brown bear first premolar teeth. Alaska Department of Fish and Game and Matson’s Laboratory, Milltown, Montana.
[16.] Matson's Laboratory. 1988. Progress report No. 10-winter 1988. Matson's Lab., Milltown, Mont.
[17.] McLaughlin, C. R., Matula Jr, G. J., Cross, R. A., Halteman, W. H., Caron, M. A., & Morris, K. I. (1990). Precision and accuracy of estimating age of Maine black bears by cementum annuli. Bears: Their Biology and Management, 415-419.
[18.] Mundy, K. R., & Fuller, W. A. (1964). Age determination in the grizzly bear. The Journal of Wildlife Management, 863-866.
[19.] Palmisciano, D. (1988). Dental characteristics relative to age in grizzly bears. Montana Dep. Fish, Wildlife and Parks working paper. Unpubl. Bozeman.
[20.] Pearson, A. M. (1976). Population characteristics of the arctic mountain grizzly bear. Bears: Their Biology and Management, 247-260.
[21.] Rogers, L. L. (1978, April). Interpretation of cementum annuli in first premolars of bears. In Proceedings of the Fourth Eastern Workshop on Black Bear Research and Management, University of Maine, Orono, Maine (pp. 102-112).
[22.] Scheffer, V. B. (1950). Growth layers on the teeth of Pinnipedia as an indication of age. Science, 112(2907), 309-311.
[23.] Stoneberg, R. P., & Jonkel, C. J. (1966). Age determination of black bears by cementum layers. The Journal of Wildlife Management, 411-414.
[24.] Thomas, D. C. (1977). Metachromatic staining of dental cementum for mammalian age determination. The Journal of Wildlife Management, 207-210.
[1.] Blanchard , B. M. (1986). Yellowstone grizzly size/growth patterns. International Conference of Bear Research and Management. 7:21-25
[2.] Carrel, W. K. (1992). Reproductive history in dental cementum of female black bears. In International Conference on Bear Research and Management (Vol. 9, No. 1, pp. 205-12).
[3.] Coy, P. L., & Garshelis, D. L. (1992). Reconstructing reproductive histories of black bears from the incremental layering in dental cementum. Canadian Journal of Zoology, 70(11), 2150-2160.
[4.] Craighead, J. J., Craighead Jr, F. C., & McCutchen, H. E. (1970). Age determination of grizzly bears from fourth premolar tooth sections. The Journal of Wildlife Management, 353-363.
[5.] Elbroch, M. (2006). Animal skulls: a guide to North American species. Stackpole Books.
[6.] Hildebrandt, T.D. 1976. Age determination in Michigan black bear by means of cementum annuli. Mich. Dep. Nat. Resour. Rep. No. 2758., Lansing.
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