Abstract
Forty male brown bear heads were non-destructively analyzed by computed tomography. Skull, frontal, and cranial cavity volumes were measured, and growth curves and regression lines were constructed. The morphological dynamics of the frontal sinus were also examined. Skull volume increased rapidly from 0 to 11 years of age, then grew more slowly until 21 years, when it plateaued. The frontal sinus also increased rapidly from 0 years, reaching approximately 300 mL by 10 years, after which growth ceased. The frontal sinus-to-skull ratio rose quickly from 0 to 4 years, then increased more gradually until 10 years, and then plateaued. Morphologically, the frontal sinus developed posteriorly to cover the anterior part of the cranial cavity, extended ventrally in the anterior lateral part of the cranial cavity and the orbital region, and protruded into the zygomatic process of the frontal bone. The cranial cavity increased slowly from 0 years, with continued growth beyond 11 years at a reduced rate. The cranial cavity-to-skull ratio decreased because the skull volume significantly increased. Both the frontal sinus and cranial cavity volumes strongly correlated with skull volume, and a well-fitting regression line was obtained. This means that the volumes of the frontal sinus and cranial cavity correlate more closely with skull volume than with age. This is the first report on the non-destructive analysis of the changes in volume and morphology of the frontal sinus and cranial cavity in male brown bears.
Keywords: cranial cavity, frontal sinus, paranasal sinus, quantification, three-dimensional analysis
INTRODUCTION
The brown bear (Ursus arctos) is a large mammal with a widespread global distribution. However, Hokkaido brown bears (U. a. yesoensis) live only in Hokkaido, Japan. Wild Hokkaido brown bears have been captured at ages of 34 years in females and 30 years in males, and the maximum lifespan of captive bears is reported to be 38 years [13]. The males reach sexual maturity from 2 to 4 years of age [16], and in females, the earliest parturition has been recorded at 4 years old [13]. Within this species, there is considerable variation in the size and shape of the external skull. Several studies have attributed this variability to biogeographical factors [1, 8, 9, 11, 19], and one study emphasized that differences in feeding resources under diverse environmental conditions appear to play a significant role [7]. Overall, skull variation is generally considered an adaptive response to differing environmental conditions. Rivrud et al. [12] noted that the evolutionary rate of head circumference size in brown bears is approximately 0.2%, which may lead to substantial changes in average trait values over hundreds of generations. Accurate assessment of the morphological changes necessitates the consideration of multiple factors such as growth and sexual dimorphism. Studies on the external skull growth of brown bears indicate that while the width of the braincase ceases to grow at an early age, the zygomatic arch and facial bones continue to develop until old age [9, 14]. Suenaga [14] hypothesized that this developmental discrepancy is closely linked to the formation of a cavity within the skull. However, current knowledge regarding morphological assessment is primarily limited to the external cranium shape, and there is a paucity of research on internal structures related to external morphological growth [2, 4, 6, 10].
The paranasal sinuses are cavities encased by bones in the skull, of which the functions remain largely unknown. Blanton and Biggs [3] proposed several possible functions, including voice resonance, humidification and warming of inhaled air, increased olfactory mucosa surface area, shock absorption, mucus secretion for nasal cavity moistening, thermal insulation, and skull weight reduction. In spotted hyenas, the frontal sinus of the paranasal sinuses evenly distributes stress on the skull during biting [15]. The frontal sinus volumes were compared among 23 carnivorous species, including brown bears, polar bears, and American black bears [4], and the cranial biomechanical functions in eight Ursidae species and four extinct cave bear subspecies were compared [10]. Nevertheless, there is a lack of research on the dynamics of frontal sinus shape and volume changes during growth. Additionally, the cranial cavity containing the brain has been overlooked.
Notably, brown bears show marked sexual dimorphism, and males have a more developed cranial size and structure, such as the frontal bone, external sagittal crest, and zygomatic arch, than females, and the male cranial morphology undergoes significant changes during growth. Therefore, as an initial focus, this study investigated male specimens and aimed to non-destructively elucidate the dynamics of frontal sinus and cranial cavity volume changes associated with growth in male brown bears by employing computed tomography (CT).
MATERIALS AND METHODS
We examined the cranial structure of 40 male brown bears (0 to 25 years of age). These specimens belong to Obihiro University of Agriculture and Veterinary Medicine (specimen code: Obihiro Pr.) and the National Museum of Nature and Science (specimen code: NSMT-M) (Table 1). Three bears among the university specimens (21, 24, and 25 years of age) were zoo individuals whose age was known. The ages of the other bears were determined based on the cementum of the dental root (lower P4) by the Hokkaido Research Organization, Hokkaido, Japan.
Table 1. Volume of each individual.
| Number | Area | Age | Frontal sinus (mL)** | Left Frontal sinus (mL) | Right Frontal sinus (mL) | Cranial cavity (mL) | Skull volume (mL) | Frontal sinus / skull volume (%) | Cranial cavity / skull volume (%) |
|---|---|---|---|---|---|---|---|---|---|
| NSMT-M60254 | Setana-cho | 0 | 48.76 | 24.24 | 24.54 | 315.53 | 768 | 6.35 | 41.08 |
| NSMT-M59550 | Urakawa-cho | 0 | 13.91 | 6.97 | 6.98 | 257.03 | 498 | 2.79 | 51.66 |
| NSMT-M59663 | shiriuchi-cho | 1 | 63.11 | 32.18 | 30.95 | 365.19 | 974 | 6.48 | 37.49 |
| NSMT-M59601 | Mori-cho | 1 | 90.71 | 46.14 | 44.59 | 344.11 | 1,037 | 8.75 | 33.18 |
| NSMT-M60230 | Samani-cho | 1 | 78.48 | 38.58 | 39.96 | 318.94 | 865 | 9.07 | 36.87 |
| NSMT-M60411 | Nanae-cho | 1 | 106.33 | 54.36 | 52.05 | 343.87 | 1,070 | 9.94 | 32.14 |
| NSMT-M59575 | Kaminokuni-cho | 2 | 137.22 | 69.71 | 67.30 | 380.13 | 1,302 | 10.54 | 29.20 |
| NSMT-M59634 | Okoppe-cho | 2 | 136.23 | 68.87 | 67.43 | 362.37 | 1,206 | 11.30 | 30.05 |
| NSMT-M59588 | Yakumo-cho | 2 | 141.93 | 72.05 | 70.10 | 330.81 | 1,179 | 12.04 | 28.06 |
| NSMT-M60524 | Shimamaki-mura | 3 | 56.23 | 27.00 | 29.23 | 310.19 | 949 | 5.93 | 32.69 |
| NSMT-M60020 | Mori-cho | 3 | 127.22 | 62.13 | 65.36 | 393.97 | 1,278 | 9.95 | 30.83 |
| NSMT-M60522 | Shimamaki-mura | 3 | 129.49 | 62.29 | 67.27 | 359.05 | 1,237 | 10.47 | 29.03 |
| NSMT-M59644 | Niikappu-cho | 4 | 113.54 | 56.71 | 56.93 | 358.70 | 1,257 | 9.03 | 28.54 |
| NSMT-M60438 | Mori-cho | 4 | 147.03 | 74.36 | 72.80 | 416.75 | 1,533 | 9.59 | 27.19 |
| NSMT-M60102 | Fukushima-cho | 4 | 178.63 | 86.83 | 92.49 | 412.94 | 1,471 | 12.14 | 28.07 |
| NSMT-M60153 | Kaminokuni-cho | 4 | 234.31 | 121.11 | 113.80 | 390.68 | 1,739 | 13.47 | 22.47 |
| NSMT-M59595 | Shiriuchi-cho | 4 | 173.42 | 87.04 | 86.54 | 383.25 | 1,519 | 11.42 | 25.23 |
| NSMT-M59909 | Yakumo-cho | 5 | 221.09 | 107.10 | 114.15 | 436.64 | 1,810 | 12.21 | 24.12 |
| NSMT-M59696 | Hakodate-shi | 5 | 110.50 | 57.99 | 52.54 | 414.76 | 1,423 | 7.77 | 29.15 |
| NSMT-M59947 | Rausu-cho | 5 | 294.45 | 148.05 | 146.58 | 449.25 | 1,775 | 16.59 | 25.31 |
| NSMT-M60435 | Yakumo-cho | 6 | 209.76 | 104.43 | 105.45 | 402.24 | 1,675 | 12.52 | 24.01 |
| NSMT-M60406 | Kyouwa-cho | 6 | 365.12 | 177.27 | 188.60 | 431.10 | 2,414 | 15.13 | 17.86 |
| NSMT-M60440 | Yakumo-cho | 6 | 280.23 | 143.28 | 137.43 | 371.68 | 2,009 | 13.95 | 18.50 |
| NSMT-M59983 | Kaminokuni-cho | 7 | 261.15 | 128.61 | 132.85 | 420.98 | 1,829 | 14.28 | 23.02 |
| NSMT-M59886 | Setana-cho | 7 | 288.25 | 138.22 | 150.35 | 454.74 | 2,202 | 13.09 | 20.65 |
| NSMT-M59980 | Mori-cho | 7 | 257.39 | 128.58 | 129.31 | 431.72 | 2,055 | 12.53 | 21.01 |
| NSMT-M60554 | Kaminokuni-cho | 7 | 365.68 | 186.27 | 180.50 | 416.40 | 2,070 | 17.67 | 20.12 |
| NSMT-M59724 | Yakumo-cho | 8 | 341.16 | 169.85 | 171.76 | 443.74 | 1,963 | 17.38 | 22.61 |
| NSMT-M59622 | Mori-cho | 8 | 281.85 | 138.87 | 143.42 | 440.53 | 1,993 | 14.14 | 22.10 |
| NSMT-M59941 | Shimamaki-mura | 8 | 406.11 | 203.63 | 204.02 | 443.45 | 2,456 | 16.54 | 18.06 |
| NSMT-M60400 | Imakane-cho | 9 | 258.37 | 130.37 | 126.61 | 396.85 | 1,895 | 13.63 | 20.94 |
| NSMT-M59837 | Kushiro-shi | 9 | 532.40 | 262.12 | 271.75 | 500.27 | 2,885 | 18.45 | 17.34 |
| NSMT-M59560 | Yakumo-cho | 9 | 260.99 | 139.47 | 122.04 | 431.82 | 1,982 | 13.17 | 21.79 |
| NSMT-M60330 | Assabu-cho | 10 | 302.82 | 147.28 | 155.99 | 392.10 | 1,819 | 16.65 | 21.56 |
| NSMT-M60335 | Assabu-cho | 11 | 233.54 | 113.15 | 121.04 | 444.03 | 1,942 | 12.03 | 22.86 |
| NSMT-M60582 | Yakumo-cho | 11 | 255.19 | 120.92 | 135.54 | 426.00 | 2,029 | 12.58 | 21.00 |
| NSMT-M60578 | Mori-cho | 11 | 252.32 | 132.78 | 119.87 | 464.48 | 2,143 | 11.77 | 21.67 |
| Pr.3824 | Zoo* | 21 | 289.58 | 143.62 | 145.99 | 524.03 | 2,963 | 9.77 | 17.69 |
| Pr.3809 | Zoo* | 24 | 296.37 | 145.77 | 150.64 | 465.15 | 2,700 | 10.98 | 17.23 |
| Pr.3799 | Zoo* | 25 | 304.24 | 152.26 | 152.03 | 523.24 | 2,882 | 10.56 | 18.16 |
*: Breeding stock at Bear Mountain, Shintokucho, Hokkaido, Japan. **: The total volume of frontal sinus obtained by summation of the right and left sinuses does not exactly match the value measured when both sides were segmented together because of a subtle difference in boundary definition and threshold setting during segmentation.
All skulls were scanned using a CT scanner (Aquilion LD, Canon, Tokyo, Japan) with the following conditions: 135 kV, 200 mA, and a slice thickness of 0.5 mm. We analyzed the internal and external cranial structure using Virtual Place Fujin software (AZE, Tokyo, Japan). The volumes of the frontal sinus, cranial cavity, and entire skull were estimated from the resulting three-dimensional (3D) models. We calculated the percentage of each internal structure volume relative to the entire skull volume. The mean for each age group (mean), standard error (SE), standard deviation (SD), coefficient of variation (CV), and maximum and minimum (Min-Max) values were determined. For visual comparison of the growth patterns, Gompertz curves (y = K·b{e{-cx}}), which had a higher coefficient of determination R2 than the other three growth curves (logistic, monomolecular, and 4 parameter logistic curves), were drawn for the volumes (Microsoft Excel 2019, Microsoft®). Moreover, regression analysis and correlation coefficients (r) were used to clarify the linear relationships between each internal structure volume and the total skull volume.
RESULTS
Details of each volume for each individual are shown in Table 1. The indicators for each volume in each age group are summarized in Tables 2, 3, 4, 5, 6.
Table 2. Age-specific means of skull volume (mL).
| Age | n | Mean | SE | SD | CV | Min–Max |
|---|---|---|---|---|---|---|
| 0 | 2 | 633 | 135.00 | 190.92 | 0.30 | 498–768 |
| 1 | 4 | 987 | 45.13 | 90.26 | 0.09 | 865–1,070 |
| 2 | 3 | 1,229 | 37.32 | 64.65 | 0.05 | 1,179–1,302 |
| 3 | 3 | 1,155 | 103.51 | 179.29 | 0.16 | 949–1,278 |
| 4 | 5 | 1,504 | 76.94 | 172.04 | 0.11 | 1,257–1,739 |
| 5 | 3 | 1,669 | 123.58 | 214.05 | 0.13 | 1,423–1,810 |
| 6 | 3 | 2,033 | 213.66 | 370.07 | 0.18 | 1,675–2,414 |
| 7 | 4 | 2,039 | 77.40 | 154.80 | 0.08 | 1,829–2,202 |
| 8 | 3 | 2,137 | 159.57 | 276.38 | 0.13 | 1,963–2,456 |
| 9 | 3 | 2,254 | 316.50 | 548.19 | 0.24 | 1,895–2,885 |
| 10 | 1 | 1,819* | - | - | - | - |
| 11 | 3 | 2,038 | 58.20 | 100.80 | 0.05 | 1,942–2,143 |
| 21 | 1 | 2,963* | - | - | - | - |
| 24 | 1 | 2,700* | - | - | - | - |
| 25 | 1 | 2,882* | - | - | - | - |
*: Actual measured value. CV: coefficient of variation.
Table 3. Age-specific means of frontal sinus volume (mL).
| Age | n | Mean | SE | SD | CV | Min–Max |
|---|---|---|---|---|---|---|
| 0 | 2 | 31.34 | 17.43 | 24.64 | 0.79 | 13.91–48.76 |
| 1 | 4 | 84.66 | 9.17 | 18.34 | 0.22 | 63.11–106.33 |
| 2 | 3 | 138.46 | 1.76 | 3.05 | 0.02 | 136.23–141.93 |
| 3 | 3 | 104.31 | 24.05 | 41.66 | 0.40 | 56.23–129.49 |
| 4 | 5 | 169.39 | 19.92 | 44.54 | 0.26 | 113.54–235.46 |
| 5 | 3 | 208.68 | 53.46 | 92.60 | 0.44 | 110.50–294.45 |
| 6 | 3 | 285.04 | 44.91 | 77.79 | 0.27 | 209.76–365.12 |
| 7 | 4 | 293.12 | 25.15 | 50.29 | 0.17 | 257.39–365.68 |
| 8 | 3 | 343.04 | 35.88 | 62.15 | 0.18 | 281.85–406.11 |
| 9 | 3 | 350.59 | 90.91 | 157.46 | 0.45 | 258.37–532.40 |
| 10 | 1 | 302.82* | - | - | - | - |
| 11 | 3 | 247.02 | 6.79 | 11.76 | 0.05 | 233.54–255.19 |
| 21 | 1 | 289.58* | - | - | - | - |
| 24 | 1 | 296.37* | - | - | - | - |
| 25 | 1 | 304.24* | - | - | - | - |
*: Actual measured value. CV: coefficient of variation.
Table 4. Age-specific means of frontal sinus/skull volume (%).
| Age | n | Mean | SE | SD | CV | Min–Max |
|---|---|---|---|---|---|---|
| 0 | 2 | 4.57 | 1.78 | 2.51 | 0.55 | 2.79–6.35 |
| 1 | 4 | 8.56 | 0.74 | 1.47 | 0.17 | 6.48–9.94 |
| 2 | 3 | 11.29 | 0.43 | 0.75 | 0.07 | 10.54–12.04 |
| 3 | 3 | 8.78 | 1.44 | 2.49 | 0.28 | 5.93–10.47 |
| 4 | 5 | 11.13 | 0.82 | 1.83 | 0.16 | 9.03–16.52 |
| 5 | 3 | 12.19 | 2.55 | 4.41 | 0.36 | 7.77–16.59 |
| 6 | 3 | 13.87 | 0.75 | 1.30 | 0.09 | 12.52–15.13 |
| 7 | 4 | 14.39 | 1.15 | 2.30 | 0.16 | 12.53–17.67 |
| 8 | 3 | 16.02 | 16.02 | 1.68 | 0.10 | 14.14–17.38 |
| 9 | 3 | 15.09 | 1.69 | 2.93 | 0.19 | 13.17–18.45 |
| 10 | 1 | 16.65* | - | - | - | - |
| 11 | 3 | 12.13 | 0.24 | 0.41 | 0.03 | 11.77–12.58 |
| 21 | 1 | 9.77* | - | - | - | - |
| 24 | 1 | 10.98* | - | - | - | - |
| 25 | 1 | 10.56* | - | - | - | - |
*: Actual measured value. CV: coefficient of variation.
Table 5. Age-specific means of cranial cavity volume (mL).
| Age | n | Mean | SE | SD | CV | Min–Max |
|---|---|---|---|---|---|---|
| 0 | 2 | 286.28 | 29.25 | 41.37 | 0.14 | 257.03–315.53 |
| 1 | 4 | 343.03 | 9.46 | 18.91 | 0.06 | 318.94–365.19 |
| 2 | 3 | 357.77 | 14.42 | 24.98 | 0.07 | 330.81–380.13 |
| 3 | 3 | 354.40 | 24.30 | 42.08 | 0.12 | 310.19–393.97 |
| 4 | 5 | 392.46 | 10.58 | 23.65 | 0.06 | 330.34–416.75 |
| 5 | 3 | 433.55 | 10.08 | 17.45 | 0.04 | 414.76–449.25 |
| 6 | 3 | 401.67 | 17.16 | 29.71 | 0.07 | 371.68–431.10 |
| 7 | 4 | 430.96 | 8.55 | 17.10 | 0.04 | 416.4–454.74 |
| 8 | 3 | 442.67 | 1.07 | 1.86 | 0.00 | 440.53–443.74 |
| 9 | 3 | 442.99 | 30.38 | 52.63 | 0.12 | 396.85–500.27 |
| 10 | 1 | 392.10* | - | - | - | - |
| 11 | 3 | 444.84 | 11.12 | 19.25 | 0.04 | 426.00–464.48 |
| 21 | 1 | 524.03* | - | - | - | - |
| 24 | 1 | 465.15* | - | - | - | - |
| 25 | 1 | 523.24* | - | - | - | - |
*: Actual measured value. CV: coefficient of variation.
Table 6. Age-specific means of cranial cavity/skull volume (%).
| Age | n | Mean | SE | SD | CV | Min–Max |
|---|---|---|---|---|---|---|
| 0 | 2 | 46.35 | 5.26 | 7.44 | 0.16 | 41.08–51.61 |
| 1 | 4 | 34.92 | 1.33 | 2.66 | 0.08 | 32.14–37.49 |
| 2 | 3 | 29.10 | 0.58 | 1.00 | 0.03 | 28.06–30.05 |
| 3 | 3 | 30.85 | 1.06 | 1.83 | 0.06 | 29.03–32.69 |
| 4 | 5 | 26.30 | 1.11 | 2.49 | 0.09 | 22.47–28.54 |
| 5 | 3 | 26.19 | 1.52 | 2.63 | 0.10 | 24.12–29.15 |
| 6 | 3 | 20.12 | 1.95 | 3.38 | 0.17 | 17.86–24.01 |
| 7 | 4 | 21.20 | 0.63 | 1.27 | 0.06 | 20.12–23.02 |
| 8 | 3 | 20.93 | 1.44 | 2.49 | 0.12 | 18.06–22.61 |
| 9 | 3 | 20.02 | 1.36 | 2.36 | 0.12 | 17.34–21.79 |
| 10 | 1 | 21.56* | - | - | - | - |
| 11 | 3 | 21.84 | 0.55 | 0.95 | 0.04 | 21.00–22.86 |
| 21 | 1 | 17.69* | - | - | - | - |
| 24 | 1 | 17.23* | - | - | - | - |
| 25 | 1 | 18.16* | - | - | - |
*: Actual measured value. CV: coefficient of variation.
Skull volume
For the entire skull volume, the minimum was 498 mL at 0 years of age, and the maximum was 2,963 mL at 21 years of age. The skull volume rapidly increased from 0 to 11 years of age, but the rate of increase decreased after 11 years of age and eventually plateaued around 21 years of age (Fig. 1a).
Fig. 1.
Growth curves of each volume with age. a: skull, b: frontal sinus, c: frontal sinus-to-skull ratio, d: cranial cavity, e: cranial cavity-to-skull ratio.
Frontal sinus
For the frontal sinus, the volume rapidly increased from 0 years of age but stopped at approximately 300 mL by 10 years of age (Fig. 1b). The frontal sinus-to-skull volume ratio rapidly increased from 0 to 4 years of age, then increased at a slower rate until 10 years of age, and plateaued after 10 years of age (Fig. 1c). Images of the frontal sinus are shown in Figs. 2, 3, 4. The frontal sinus developed almost symmetrically and posteriorly to cover the braincase, age-dependently. Furthermore, the frontal sinus protruded into the zygomatic process (orange arrow) and orbital area (green arrow), and along the anterior wall of the cranial cavity (yellow arrow) (Fig. 4).
Fig. 2.
3D extracted CT image of the frontal sinus in brown bears (dorsal view). Yellow and green numbers indicate the maximum cranial length and total frontal sinus volume, respectively. The external occipital protuberance is aligned with the dashed line. Red and blue denote the left and right frontal sinus, respectively. Pink indicates the cranial cavity.
Fig. 3.
3D extracted CT image of the frontal sinus in brown bears (left lateral view). Yellow and green numbers indicate the basal length and total frontal sinus volume. The posterior edge of the occipital condyle is aligned with the dashed line. Red denotes the left frontal sinus.
Fig. 4.
Frontal sinus distribution in brown bears. Comparison of 3D images and skeletal specimens. A: right lateral view, B: right dorsolateral view, C: dorsal view; 1: skeletal specimen, 2: 3D image (blue, right frontal sinus; red, left frontal sinus; pink, cranial cavity). White arrow, tip of zygomatic process of frontal bone; red arrow, tip of frontal process of zygomatic bone; yellow arrow, frontal sinus extending ventrally in the anterior lateral part of the cranial cavity (corresponding area in the skeletal specimen); green arrow, frontal sinus extending ventrally in the orbital region (corresponding area in the skeletal specimen); orange arrow, tip of frontal sinus extending to the zygomatic process of frontal bone. esc, external sagittal crest; fb, frontal bone; fbs, facial bones; nc, nuchal crest; zp, zygomatic process of temporal bone. Specimen no. Pr. 3799.
Cranial cavity
For the cranial cavity, the volume slowly increased from 0 years of age and continued to grow at a slower rate after 11 years of age (Fig. 1d). The cranial cavity-to-skull volume ratio gradually decreased from approximately 40% and stabilized at approximately 20% after 10 years of age (Fig. 1e). Images of the cranial cavity are shown in Figs. 5 and 6. Age-related growth of the facial bones, frontal bone, external sagittal and nuchal crests, and zygomatic process of the temporal bone was notable compared with that of the cranial cavity (Figs. 4, 5, 6).
Fig. 5.
3D extracted CT image of the cranial cavity in brown bears (dorsal view). Yellow and green numbers indicate the maximum cranial length and cranial cavity volume, respectively. The posterior edge of the cranial cavity is aligned with the dashed line. Pink indicates the cranial cavity. White arrow, zygomatic process of the temporal bone; blue arrow, frontal bone; yellow arrow, nuchal crest.
Fig. 6.
3D extracted CT image of the cranial cavity in brown bears (left lateral view). Yellow and green numbers indicate the basal length and cranial cavity volume, respectively. The posterior edge of the cranial cavity is aligned with the dashed line. Pink indicates the cranial cavity. White arrow, external sagittal crest.
Regression analysis
Frontal sinus and cranial cavity volume showed a high positive correlation with skull volume (frontal sinus: r=0.898; cranial cavity: r=0.921), and a regression line with good fit was obtained (Fig. 7).
Fig. 7.
Regression lines for the frontal sinus and cranial cavity volumes relative to the skull volume. Circles (○) and squares (□) denote the cranial cavity and frontal sinus, respectively.
DISCUSSION
In morphological studies of brown bears, the external shape has been extensively studied, but less is known about the internal shape [2, 4, 6, 10]. By leveraging CT, we non-destructively quantified the cranial internal structure of the brown bear. The present study is the first to quantitatively and qualitatively reveal the dynamics of the internal structure of brown bears.
Two grizzly bears (age unknown), a subspecies of brown bear, had an average frontal sinus volume of 152.0 mL [4]. Based on our growth curve, this corresponds to the frontal sinus volume of a 3–4-year-old, suggesting that the bears were not fully grown. Therefore, this value should not be considered standard for the frontal sinus volume in adult brown bears. Furthermore, García et al. [6] measured the frontal sinus volumes of seven adult brown bears, without determining their ages, and reported a range of 97.57 to 302.95 mL. Based on the results of the growth curves in the present study, it can be inferred that the six individuals were between 2 and 7 years of age, and the individual showing the maximum volume was approximately 10 years or older. However, because the Hokkaido brown bears measured in this study are a small species among brown bear subspecies, it is necessary to consider the possibility that this growth curve is unique to the population. In addition, all three of the older individuals examined in this study had been kept in the zoological park their entire lives, and their growth curves for the frontal sinus-to-total skull volume ratio showed values that were lower than the expected line. These three individuals were fed compound feed or dog food that had been softened with water, and compared with wild individuals, they likely had fewer opportunities to eat hard food daily. Tanner et al. [15] reported that the frontal sinuses evenly dissipate the stress applied to the skull during occlusion, and thus, it is possible that the frontal sinuses of the three aged individuals used in the analysis were less developed than those of their wild counterparts. However, no differences were reported in the development of cranial morphology, including frontal sinuses, between captive-reared and wild coyotes [5]. Nonetheless, the differences due to rearing environment in the brown bear cannot be easily verified because older individuals, such as those used in this study, are particularly difficult to find and obtain from the wild.
The frontal sinus of the bear grows large over a long period, from an underdeveloped state. The frontal sinus is surrounded by the frontal bone, which may be involved in increasing the attachment area of the masticatory muscles [3]. The zygomatic arch, where Suenaga [14] pointed out a discrepancy in growth with the width of the braincase, is also related to the mass of the masticatory muscles. Therefore, the development of the frontal sinus may be involved in the increase in the attachment area of the masticatory muscles and the dispersion of applied masticatory force.
In the cranial cavity, Veitschegger [17] estimated the brain volume of 93 brown bears using the glass bead method, showing that the minimum value was 250 mL and the maximum value was 520 mL. In the present study, the minimum cranial cavity volume was 257.03 mL at 0 years of age, the maximum was 524.0 mL at 21 years, and the range of volumes is nearly consistent with that observed by Veitschegger [17]. In the growth pattern, the cranial cavity that houses the brain had already grown to a certain extent at the age of 0 years, and thereafter, showed slow growth. Conversely, the entire skull volume rapidly increased until 11 years of age, and after that, the increase rate decreased. Therefore, the cranial cavity-to-skull volume ratio gradually decreased from approximately 40% and finally stabilized at approximately 20%. Suenaga [14] reported that the greatest breadth of the braincase, which is related to brain development, reaches its maximum at around 12 months of age and suggested that the growth of the braincase stops while other compartments of the skull continue to develop. However, in our 3D analysis, the cranial cavity volume continued to increase with a low growth rate even after 1 year (12 months) of age, and marked continuous growth of the skull components around the braincase was also observed. Therefore, 3D analysis is important for conducting accurate cranial examinations.
In the regression analysis, the volumes of the frontal sinus and cranial cavity were found to increase in correlation with the cranium volume, not necessarily in correlation with age. Even when ages differ, comparable cranial volumes suggest that the volumes of the frontal sinus and cranial cavity are also likely to be similar. In other words, even among individuals of the same age, variations in the degree of cranial development reflecting individual differences in growth can influence both the frontal sinus and cranial cavity volumes. While individual variability in growth is commonly observed across animal species, the establishment of a more reliable and representative growth curve requires the inclusion of a larger number of specimens within each age group, despite the significant challenges associated with acquiring older individuals.
In conclusion, this is the first report on the non-destructive CT analysis of volume and morphology changes in the frontal sinuses and cranial cavities of male brown bears, and the growth curves and regression lines of the frontal sinuses and cranial cavities were revealed. Furthermore, the morphological dynamics of the frontal sinuses and positional relationship of the cranial cavities within the skull were clarified. In the Ursidae, other paranasal sinuses, such as the maxillary and sphenoidal sinuses, have been reported [10, 18]. However, the detailed 3D structure and its dynamics during growth are not well known. Further studies are needed to examine the characteristics of the other two paranasal sinuses, in addition to the dynamics of female frontal sinuses with growth. Moreover, along with classical external measurements, we plan to non-destructively measure the internal structures related to the sinuses imaged by CT and analyze the correlations among age, sinus volume, and measurement type. This analysis may allow us to infer 3D skull growth, including the sinuses, from two-dimensional measurements.
CONFLICTS OF INTEREST
The authors declare no conflicts of interest.
Acknowledgments
We extend our gratitude to the Hokkaido Research Organization for their efforts in collecting the specimens and individual data. Our sincere appreciation goes to Sahoro Resort Bear Mountain for supplying specimens. We are also indebted to Dr. S. Kawada for his meticulous organization of the collection process. This work was supported by the Inui Tasuke Scientific Foundation.
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