# Skull Shape Diversity in Pet Rabbits and the Applicability of Anatomical Reference Lines for Objective Interpretation of Dental Disease

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## Abstract

**:**

## 1. Introduction

## 2. Materials and Methods

#### 2.1. Data Set and Radiographic Screening

#### 2.2. Linear Morphometrics

_{10}-transformed and size-normalized to ensure that variation could be attributed to shape differences, rather than size differences. The log

_{10}-transformed data (except the measured angles) were regressed against log

_{10}-transformed maximal cranial length for each specimen. The resulting residuals, i.e., the size-normalized measurements, were used for the subsequent statistical analyses.

#### 2.3. Geometric Morphometrics

#### 2.4. Statistical Analyses

## 3. Results

#### 3.1. Linear Morphometrics

#### 3.2. Skull Length and Height

#### 3.3. Nasal Height

#### 3.4. Palatal and Facial Tilt Angle

#### 3.5. Occipital Angle

#### 3.6. Geometric Morphometrics

_{N}= 0.0029) than in group Y (MD

_{Y}= 0.0017). Specimens of group N cover a slightly larger area of the morphospace in contrast to specimens of group Y (Figure 7). The difference is statistically significant (p = 0.002).

## 4. Discussion

#### 4.1. Skull Shape Diversity in Pet Rabbits

#### 4.2. Evolutionary Transformations of the Rabbit Skull

#### 4.3. Skull Development and Palate

#### 4.4. Outlook: Breeding for Good Dental and Oral Health

## 5. Conclusions

## Author Contributions

## Funding

## Conflicts of Interest

## References

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**Figure 1.**Example highlighting the importance to integrate effective, noninvasive techniques, such as radiography, in the clinical examination routine. (

**A**) Rostrocaudal view of an apparently healthy dentition in a pet rabbit with mouth closed and (

**B**) opened. (

**C**) Lateral view of the skull with applied anatomical reference lines according to Böhmer and Crossley [11]. The yellow line begins at the rostral end of the hard palate immediately caudal to the second incisor and extends caudally to pass through the tympanic bulla at approximately one-third of its height. In healthy pet rabbits, it marks the physiological occlusal plane between maxillary and mandibular molars. In the present specimen, the occlusal line depicts a slight elongation of the clinical crown of the first lower cheek tooth (P3) which might be missed on clinical examination alone (see A and B). (

**D**) The laterolateral X-ray is the gold standard to detect that this rabbit suffers from an early stage of malocclusion. The overlong mandibular P3 progressively bends rostrally causing a widening of the approximal space to the adjacent P4 (arrow). Due to the abnormally short clinical crown of the antagonist (maxillary P2), the occlusal plane of the cheek teeth shows a subtle caudal slant (red dashed line).

**Figure 3.**Results of the principal components (PC) analyses. (

**A**,

**B**) Scatterplot and contributions of the variables considering all measurements. (

**C**,

**D**) Scatterplot and contributions of the variables considering linear measurements only. The percentage of explained variances by each PC is indicated in parentheses. Arrows represent the squared loadings of the variables and the color intensity is proportional to the value of the loading. Variables that are closer to the correlation circle contribute more to the principal components.

**Figure 4.**Variance in palatal angle and facial tilt angle. (

**A,C**) Boxplot and (

**B,D**) schematic visualization of the mean angle for each group. Both, the palatal angle and the facial tilt angle, are significantly different between group Y and group N. (

**C**) The variance in facial tilt angle among leporids (data from Kraatz et al. [23]) lies within the combined variance observed in pet rabbits (this study).

**Figure 5.**Relation between facial tilt angle and palatal angle. (

**A**) Linear regression considering all data. (

**B**) Linear regression considering the two groups separately.

**Figure 6.**Variance in occipital angle. (

**A**) Boxplot and (

**B**) schematic visualization of the mean angle for each group. It is significantly different between group Y and group N (p = 0.003). (

**C**) Relation between occipital angle and maximal cranial length to height ratio.

**Figure 7.**Results of the geometric morphometric analysis. The scatterplot displays the distribution of the sampled specimens in the morphospace represented by the first two principal components (PC1 and PC2). The percentage of explained variance by each PC is indicated in parentheses. The outlines visualize the shape differences between the extreme configurations (min = minimum, max = maximum) along PC1 and PC2.

**Figure 8.**Cranial flexion in rodents and the sister taxon lagomorphs (ochotonids and leporids). The red line represents the orientation of the basicranium. The green line indicates the palatal plane. The white line shows the orientation of the occiput and the foramen magnum. (

**A**) Rat (rodent). (

**B**) Pika (ochotonid). (

**C**) Wild rabbit (leporid). (

**D**) Pet rabbit (leporid). Note the pronounced flexion in lagomorphs. The skulls are scaled to same length and oriented with the cranial base plane being horizontal.

**Table 1.**Definition of the established measurements and planes used in the linear morphometric analysis. The linear measurements and the angles were obtained on laterolateral X-ray images of the skull. Refer also to Figure 2A.

Linear Measurement | Definition |
---|---|

Caudal nasal height | Distance (perpendicular to the nasal plane) between the caudal nasal roof and the palate (at the rostral intersection between maxillary bone and first maxillary cheek tooth P2) |

Maximal cranial length | Maximal distance between the most rostral end of the upper incisor and the occipital protuberance (crossing the most rostral point of the hard palate) |

Maximal cranial height | Maximal distance between the mandibular facial incisure to the most dorsal point of the frontal bone |

Maxillary molar length | Maximal distance between the first maxillary cheek tooth P2 and the last maxillary molar M3 |

Palatal length | Distance between the most rostral end of the palate (at the intersection between second maxillary incisor I2 (peg tooth) and maxillary bone) and the rostral intersection between maxillary bone and first maxillary cheek tooth P2 |

Rostral nasal height | Distance (perpendicular to the nasal plane) between the rostral nasal roof (at the most rostral end of the nasal bone) and the palate |

Plane | |

Nasal plane | Tangent to the nasal bone |

Occipital plane | Tangent to the occiput (great foramen) |

Palatal plane | Tangent to the hard palate (without its most rostral part which slopes downwards) |

Skull base plane | Line connecting the rostral end of the hard palate immediately caudal to the second incisor and the ventral border of the tympanic bullae |

Angle | |

Facial tilt angle | Angle between the palatal plane and the occipital plane |

Nasal angle | Angle between the nasal plane and the skull base plane |

Occipital angle | Angle between the occipital plane and the skull base plane |

Palatal angle | Angle between the palatal plane and the skull base plane |

# | Type | Definition |
---|---|---|

LM | ||

1 | II | Most rostral point of nasal bone |

2 | I | Intersection between nasal bone and rostral orbital roof |

3 | I | Intersection between frontal bone and caudal orbital roof |

4 | II | Most caudal point of occipital protuberance |

5 | II | Most caudal point of tympanic bulla |

6 | II | Most dorsal point of tympanic bulla |

7 | II | Most rostral point of tympanic bulla |

8 | II | Most ventral point of tympanic bulla |

9 | III | Center of temporomandibular joint |

10 | I | Caudal intersection between maxillary bone and last maxillary molar M3 |

11 | I | Rostral intersection between maxillary bone and first maxillary cheek tooth P2 |

12 | I | Intersection between second maxillary incisor I2 (peg tooth) and premaxillary bone |

13 | I | Rostral intersection between first maxillary incisor I1 and premaxillary bone |

SemiLM | ||

14–23 | - | Nasal bone (curve between LM1 and LM2) |

24–28 | - | Orbital roof (curve between LM2 and LM3) |

29–38 | - | Dorsal braincase (curve between LM3 and LM4) |

39–43 | - | Occiput (curve between LM4 and LM5) |

44–48 | - | Palate (curve between LM11 and LM12) |

Group Y vs. Group N | F Value | p-Value |
---|---|---|

Palatal angle | 90.654 | <0.0001 * |

Caudal nasal height | 46.971 | <0.0001 * |

Facial tilt angle | 43.599 | <0.0001 * |

Maximal cranial height | 42.792 | <0.0001 * |

Maxillary molar length | 6.6609 | 0.01 * |

Rostral nasal height | 6.1633 | 0.01 * |

Nasal bone angle | 0.6396 | 0.4263 |

Maximal palatal length | 0.2096 | 0.6483 |

l/h Ratio | Group Y (N = 58) | Group N (N = 22) |
---|---|---|

Minimum | 3.05 | 2.8 |

Mean | 3.40 | 3.11 |

Maximum | 3.74 | 3.68 |

Variance | 0.03 | 0.05 |

**Table 5.**Results of the k-means cluster analyses testing the variables that contribute most to the group differentiation in the linear morphometric morphospace.

Variable | Correctly Assigned to Group N | Correctly Assigned to Group Y |
---|---|---|

Rostral nasal height | 22.7% | 51.7% |

Caudal nasal height | 81.8% | 82.8% |

Facial tilt angle | 77.3% | 62.1% |

Palatal angle | 100% | 87.9% |

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**MDPI and ACS Style**

Böhmer, C.; Böhmer, E. Skull Shape Diversity in Pet Rabbits and the Applicability of Anatomical Reference Lines for Objective Interpretation of Dental Disease. *Vet. Sci.* **2020**, *7*, 182.
https://doi.org/10.3390/vetsci7040182

**AMA Style**

Böhmer C, Böhmer E. Skull Shape Diversity in Pet Rabbits and the Applicability of Anatomical Reference Lines for Objective Interpretation of Dental Disease. *Veterinary Sciences*. 2020; 7(4):182.
https://doi.org/10.3390/vetsci7040182

**Chicago/Turabian Style**

Böhmer, Christine, and Estella Böhmer. 2020. "Skull Shape Diversity in Pet Rabbits and the Applicability of Anatomical Reference Lines for Objective Interpretation of Dental Disease" *Veterinary Sciences* 7, no. 4: 182.
https://doi.org/10.3390/vetsci7040182