THE ANATOMICAL RECORD PART A 272A:460 – 466 (2003) On the Variability of Skull Shape in German Shepherd (Alsatian) Puppies VEDAT ONAR1* AND HALİL GÜNEŞ2 Department of Anatomy, Faculty of Veterinary Medicine, Istanbul University, Istanbul, Turkey 2 Department of Animal Breeding, Faculty of Veterinary Medicine, Istanbul University, Istanbul, Turkey 1 ABSTRACT In this study the skulls of 32 German shepherd puppies (40 –107 days old) were examined. They were divided into three age groups (40 – 49, 50 – 69, and 70 –107 days) and the variability of their shapes was determined. Some geometrical shapes were drawn by joining the measuring points. Angle measurements were made on these shapes, which comprised the whole skull, neurocranium, and viscerocranium. The skull index was further calculated in order to assess the correlation, if any, of this index with the angle measurements. It was found that the length of the skull increased more than the width, and, accordingly, the skull became narrower and longer with age. Furthermore, the AZP and AZN angles widened with age, while the ZAZ, ZPZ, NcANc, NcPNc, NcBrNc, SwNSw, and SwPSw angles decreased. The decrease in the skull index, which was not proportionate to the age, showed that the zygomatic width did not increase as much compared to the length of the skull. Anat Rec Part A 272A:460 – 466, 2003. © 2003 Wiley-Liss, Inc. Key words: German shepherd dog; skull; angle; measurements; geometry Skulls differ more in size and shape among domestic dogs than in any other mammalian species (Evans, 1993; Vilà et al., 1999). The shape of the skull in dogs shows considerable breed and individual variations in form and size (Sisson, 1975). It is the most important criterion in determining the standard breeds of dogs, and skull indices and ratios are effective tools for separating and deﬁning the morphological types. For this reason, canine skull forms have been the subject of many studies (Stockard, 1941; Komeyli, 1984; Brehm et al., 1985; Regedon et al., 1991, 1992; Lignereux et al., 1991; Onar et al., 2001). Morphometric measurements such as made in this study can aid in classifying skulls morphologically, detecting skull deformations, and determining the cause of those deformations. Many studies on canine skull morphometry have been performed (Hidaka et al., 1998; Kauhala et al., 1998; Onar, 1999; Onar et al., 1997, 2001; Yıldız et al., 1993), and have yielded morphometric values relevant to the skull shape. In addition, the skulls of adult dogs have been analysed biometrically, and skull bases have been examined (Huber and Lüps, 1968, 1970; Lüps and Huber, 1968, 1969a,b; Huber, 1974; Lüps, 1974; Nussbaumer, 1978, 1985). © 2003 WILEY-LISS, INC. Other studies have dealt with genetic and environmental effects on the shape of adult dog skulls (McKeown, 1974; Jouve et al., 2001). These studies utilized angular measurements of the whole skull in order to assess the changes in skull shape that occur during growth. As a result, it was concluded that environmental factors have an insigniﬁcant effect on the skull shape of adult dogs. However, the same factors were reported to have some effect on the size of skull (McKeown, 1974). It has been suggested that since dog breeds present a spectacular intraspeciﬁc polymorphism (from Yorkshire terriers to Dobermans), the dog genome can generate various ontogenies, which makes it possible to identify the differences in shape among these breeds (Jouve et al., 2001). *Correspondence to: Dr. Vedat Onar, Istanbul University, Faculty of Veterinary Medicine, Department of Anatomy, 34854, Avcilar, Istanbul, Turkey. E-mail: email@example.com Received 24 August 2001; Accepted 13 January 2003 DOI 10.1002/ar.a.10052 VARIABILITY OF SKULL SHAPE IN ALSATIANS Fig. 1. Measuring points and geometric shapes. a: Category 1. The ﬁrst shape as viewed from the prosthion point. b: Category 1. The second shape as viewed from the nasion point. A, akrokranion; N, nasion; P, prosthion; Z, zygion. While a number of studies have been performed on the geometrical morphometries of adult dogs, only a few have focused on the skulls of puppies. In the present study the skulls of German shepherd puppies, a subspecies of Alsatian canid, were studied. The morphometry of the skull and geometry of the mandibula in German shepherd dogs (a dolichocephalic breed) up to the age of 105 days were examined (Onar, 1999; Onar et al., 1999). German shepherd puppies have a wide, circular neurocranium, and a wider zygomatic width than the total skull length at birth. As they grow older, however, some morphological changes occur in the skull, such as the manifestation of an external sagittal crest and external occipital protuberance. By making use of angular measurements, the ontogenetic variations that occur in the geometrical morphometry of skulls up to the age of 107 days were examined in this study. MATERIALS AND METHODS In this study, the skulls of 32 German shepherd puppies (40 –107 days old) were examined. Puppies from different parents were obtained at different times from various dog kennels (including the Academy Dog Kennel, the International Kennel K-9 Academy, and others) situated in or around Istanbul. These puppies had died of various viral infections in the above-mentioned kennels during the period of 1997–2000. As the number of puppies was limited, it was not possible to carry out the survey for each sex separately. After the soft tissues and muscles were removed, the skulls were macerated (Onar, 1999). The skulls were divided into three age groups (40 – 49 days, n ⫽ 14; 50 – 69 days, n ⫽ 10; and 70 –107 days, n ⫽ 8) in order to determine the variability of the skull shapes. In the process of forming the groups, the closeness of the morphometric values and a small standard deviation (S.D.) were taken into consideration. Some geometrical shapes were drawn by joining the measuring points on the skulls in an attempt to assess the variations of each skull. The measuring points were marked on the skulls as follows (Von den Driesch, 1976; Evans, 1993; Onar, 1999) (Figs. 1– 4): 461 Fig. 2. Measuring points and geometric shapes continued. a. 2. a: Category 2. The ﬁrst shape as viewed from the prosthion point, and the third shape as viewed from the bregma point. b: Category 2. The second shape as viewed from the nasion point. A, akrokranion; Br, bregma; E, euryon; N, nasion; P, prosthion. Akrokranion (A): central surface point on the external occipital protuberance. Bregma (Br): median point of the parietofrontal suture. Ectorbitale (Ec): the most lateral point of the frontal bone on the occipital side of the orbit. Entorbitale (En): the naso-medial indentation of the orbit. Euryon (E): the most lateral point of the brain case. Nasion (N): junction on the median plane of the right and left nasofrontal sutures. Prosthion (P): anterior end of the interincisive suture, located between the roots of the upper central incisor teeth. Zygion (Z): the most lateral point of the zygomatic arch. Lateral point of the nose (Sw): the most lateral point of the caudal edge of the alveolus premolar 2. In the process of forming the geometrical shapes, each skull was ﬁrst photographed in the dorsal position. The pictures were then scanned and transferred to a computer. Finally, the geometric shapes were drawn by joining the aforementioned measuring points. The angles that emerged from these drawings were measured. The results from each group were evaluated separately. Thus, the variability with age of the degrees of these angles was inspected closely. The inspection demonstrated how the skull of a German shepherd puppy changes as it grows to adulthood. The geometrical shapes were divided into four categories for analysis: 1) geometric analysis based on zygion points, 2) geometric analysis based on euryon points, 3) geometric analysis based on the narrowest lateral points of the nose, and 4) geometric analysis based on the skull index. The ﬁndings were as follows. Category 1: Two different geometrical shapes were formed by taking the akrokranion as the aboral point: a) the ﬁrst shape as viewed from the prosthion point (Fig. 1a), and b) the second shape as viewed from the nasion point (Fig. 1b). Category 2: Three 462 ONAR AND GÜNEŞ Category 3: Two different geometrical shapes were formed in this category: a) the ﬁrst shape as viewed from the prosthion and nasion points (Figs. 3a), and b) the second shape as viewed from the euryon, ectorbitale, entorbitale, and zygion points (Figs. 3b). Category 4: The correlation between skull index and angle measurements was analysed in this category. The skull measurements used in the study were as follows: skull length (SL) ⫽ akrokranion (A)–prosthion (P); maximum zygomatic width (MZW) ⫽ euryon (E)– euryon (E); and skull index (SI) ⫽ maximum zygomatic width (E–E) ⫻ 100/skull length (A–P). Following this categorisation, the angles of the geometrical shapes were measured and their correlation with age was studied. To assess the variability that occurs with age, we attempted to reveal all the features of the skull, neurocranium, and viscerocranium in forming the geometric shapes. The statistical analysis in the study was based on the method of Evrim and Güneş (1998). Fig. 3. Measuring points and geometric shapes. a: Category 3. The ﬁrst shape as viewed from the prosthion and nasion points. b: Category 3. The second shape as viewed from the euryon, ectorbitale, entorbitale, and zygion points. E, euryon; Ec, ectorbitale; En, entorbitale; N, nasion; P, prosthion; Z, zygion; Sw, lateral point of the nose. RESULTS The mean values and S.D.’s of the angle measurements of each group were determined, and the variability-withage values are presented in Table 1. The correlation of the angle measurements to the skull index, and of one angle measurement to another were also calculated. The statistically signiﬁcant ﬁndings, which were grouped and analysed in four different categories, are presented below and separately in Tables 2 and 3. It was observed that the puppies in the ﬁrst group had a wide, circular neurocranium. The zygomatic width in these puppies was wider compared to the total skull length (Fig. 4A). Morphological changes in the second group began to occur as the puppies grew older. The increase in the zygomatic width of the second group was not in proportion to the skull length (Fig. 4B). In the third group, the external sagittal crest and external occipital protuberance began to manifest themselves in the dorsal crania (Fig. 4C and D). The ontogenetic variations that occurred in the skulls of these puppies are shown in schematic diagrams (drawn for each group separately) in Figure 4. Category 1 Examination of the shapes in this category revealed that while the angles of AZP and AZN became wider, those of ZAZ, ZNZ, and ZPZ decreased in degree with age. Shape “a”—prosthion taken as the point of origin. A highly negative correlation of statistical signiﬁcance was found to exist among the angles of AZP, ZAZ, and ZPZ, which remained unchanged with age. Shape “b”—nasion taken as the point of origin. Fig. 4. Schematic diagrams for each group separately: (A) 40-dayold puppy, (B) 50-day-old puppy, (C) 70-day-old puppy, and (D) 107day-old puppy. Another highly negative correlation, which was only signiﬁcant in the 50 – 69-day-old group, was discovered between the angles of AZN and ZNZ. Category 2 different geometrical shapes were formed by taking the akrokranion as the aboral point: a) the ﬁrst shape as viewed from the prosthion point (Fig. 2a), b) the second shape as viewed from the nasion point (Fig. 1b), and c) the third shape as viewed from the bregma point (Fig. 2a). It was observed that in contrast to the increase in ANcP and ANcN angles, the NcANc, NcPNc, and NcNNc angles decreased in degree as the puppies grew older. The NcBrNc angle, which had reached its highest degree in the 50 – 69-day-old group, dropped to its lowest in the 70 –107day-old group. However, the ANcBr angle, which re- 463 VARIABILITY OF SKULL SHAPE IN ALSATIANS TABLE 1. Angle measurements of the skulls of the three groups 40–49 days old ZAZ ZNZ ZPZ AZN AZP NcANc NcBrNc NcNNc NcPNc ANcBr ANcN ANcP SwNSw SwPSw NSwP ZSwP ZSwN ZSwEn EcEnSw NcEcEn SL (mm) MZW (mm) SI 50–69 days old 70–107 days old n Mean SD. n Mean SD. n Mean SD. 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 79,25 92,56 50,30 94,09 115,22 99,67 141,53 57,51 33,80 59,40 101,12 113,26 93,66 55,81 105,26 175,32 69,96 28,40 140,44 155,01 110,10 65,72 59,69 1,378 2,970 1,372 1,554 0,942 3,939 8,855 2,612 1,690 4,088 2,857 2,393 7,458 2,395 3,652 1,797 3,641 2,593 4,481 1,656 6,488 3,974 0,778 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 77,82 91,34 47,70 95,42 117,27 95,76 146,88 53,80 30,74 58,68 105,22 116,75 89,40 54,48 108,06 174,37 66,31 29,72 140,10 158,19 126,05 71,67 56,91 3,149 2,599 1,140 2,111 1,944 3,366 7,530 3,107 1,383 2,680 2,193 1,825 5,293 1,998 3,322 1,196 2,831 1,531 2,639 3,301 5,369 2,138 1,892 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 75,56 89,25 42,63 97,59 120,85 89,28 131,33 48,55 26,03 68,10 109,49 120,75 72,38 49,43 119,10 174,53 55,36 26,66 147,93 161,06 153,14 79,63 52,27 3,105 4,420 2,940 1,813 2,380 9,946 8,332 2,488 2,329 4,957 3,488 3,538 10,056 3,195 5,240 2,981 7,235 3,331 6,369 2,061 17,201 4,816 3,209 TABLE 2. Correlation analysis of the described features in German shepherd dog (Alsatian) puppies Age ZPZ AZN AZP NcBrNc NcNNc NcPNc ANcBr 40–49 50–69 70–107 40–49 50–69 70–107 40–49 50–69 70–107 40–49 50–69 70–107 40–49 50–69 70–107 40–49 50–69 70–107 40–49 50–69 70–107 ZAZ ZNZ ZPZ AZN AZP NcANc NcBrNc NcNNc 64,43* ⫺78,92** ⫺68,72** ⫺97,16*** ⫺77,46* ⫺89,83*** ⫺66,81* ⫺71,90* ⫺75,81** ⫺82,75* ⫺68,39** ⫺80,45** ⫺76,28* 84,65** ⫺77,54** ⫺63,94* 79,80** 58,65* 69,78* 77,11* ⫺80,42* ⫺79,50* ⫺85,96** 87,18** 79,54*** 89,70*** 96,18*** ⫺89,60*** ⫺91,80*** ⫺70,81* ⫺85,36** *P ⬍ 0.05; **P ⬍ 0.01; ***P ⬍ 0.001. mained constant in the ﬁrst two groups, was observed to increase in the third group of 70 –107-day-old puppies. Shape “a”—prosthion taken as the point of origin. An analysis of the angles in this geometric shape showed that ANcP had a highly negative correlation with NcANc and NcPNc. The correlation remained constant with age. In the group of 50 – 69-day-old puppies, it was signiﬁcant between ANcP and NcANc. However, the signiﬁcance shifted to the correlation between ANcP and NcPNc in the 70 –107-day-old group. Shape “b”—nasion taken as the point of origin. No correlation of statistical importance was observed between NcANc and NcNNc. However, a highly negative correlation between NcANc and ANcN was signiﬁcant in the 40 – 49-day-old and 50 – 69-day-old groups. The correlation lost its signiﬁcance in the 70 –107-day-old group. Shape “c”— bregma taken as the point of origin. NcBrNc correlated highly negatively and signiﬁcantly with ANcBr, and the degree of correlation remained the same in all three groups. NcBrNc had a similar correlation with NcANc in the 50 – 69-day-old group, whereas the correlation of NcANc and ANcBr in the same group was not found to be signiﬁcant. Category 3 It was noted in this category that the SwNSw, SwPSw, and ZSwN angles reduced in degree with age. However, TABLE 3. Correlation analysis of the described features in German shepherd dog (Alsatian) puppies continued Age ZAZ ZNZ ZPZ AZN AZP NcANc 40–49 ⫺92.39*** 50–69 ⫺70.84** 70–107 ⫺72.56* 81.64* ANcP 40–49 ⫺94.33*** 50–69 ⫺92.55*** 70–107 80.81* SwNSw 40–49 50–69 70–107 84.07** ⫺79.86* 40–49 SwPSw 50–69 72.30* 69.25* ⫺71.80* ⫺78.75** 70–107 ⫺80.52* 78.47* NSwP 40–49 50–69 ⫺67.04* 70.55* 70–107 ⫺88.68** ZSwP 40–49 50–69 70–107 84.48** ⫺90.99** 78.60* ZSwN 40–49 50–69 65.98* 70–107 87.41** ⫺85.46** ZSwEn 40–49 50–69 70–107 80.50* EcEnSw 40–49 70.48** 50–69 ⫺67.44* 72.01* 69.04* 70–107 NcEcEn 40–49 50–69 ⫺69.29* 66.72* 70–107 SI 40–49 ⫺58.31* 50–69 65.85* 63.23* 86.80** ⫺88.05*** ⫺78.40** 70–107 85.70** ⫺93.65** ANcN *P ⬍ 0.05; **P ⬍ 0.01; ***P ⬍ 0.001. NcNNc NcPNc ANcBr ⫺59.88* ⫺64.44* ⫺64.22* ⫺81.13* ⫺89.64** ⫺63.37* ⫺76.46* ⫺87.44** 63.13* 62.56* 84.85** ANcN ⫺80.96* SwPSw NSwP 81.12* ⫺87.86** ⫺83.89** ⫺81.74* 56.94* 58.14* ⫺81.14* 74.92* 95.97*** ⫺82.63* 99.26*** ⫺76.55** 63.13* 85.42** ⫺73.01* ZSwN ZSwEn EcEnSw ⫺84.89*** ⫺74.91 97.73*** ⫺93.67*** ⫺89.46*** ⫺93.28*** 89.36** ⫺74.76* 72.38* ZSwP ⫺83.09* ⫺94.75*** ⫺96.92*** ⫺75.77** ⫺95.24*** ⫺75.56* 87.57** SwNSw 97.17*** 89.65*** 99.54*** ⫺63.55* ⫺69.56** 74.41* ANcP ⫺80.78* ⫺82.28* 54.30* 67.91* ⫺64.61* 75.96** 91.85** 63.98* 79.68* ⫺57.77* ⫺84.15** 80.41** ⫺84.07** ⫺92.28** 83.08* 86.45** ⫺64.30* 95.13*** 71.27* 66.54* VARIABILITY OF SKULL SHAPE IN ALSATIANS the increment in the angles of NcEcEn and NSwP was in proportion to the increase in age. While the change of ZSwP with age was insigniﬁcant, that of ZswEn (in which the degree of the angle was largest in the 50 – 69-day-old group) was signiﬁcant. EcEnSw remained constant in the 40 – 49- and 50 – 69-day-old groups, but it increased in the group of 70 –107-day-old puppies. Shape “a”—prosthion and nasion taken as the points of origin. A highly negative correlation that remained unchanged with age was observed between the angles of SwNSw and NSwP. This was considered to be signiﬁcant. A similar correlation in the 50 – 69-day-old group was present between the angles of SwPSw and NSwP. Shape “b”— euryon, ectorbitale, entorbitale, and zygion taken as the points of origin. The correlation between SwPSw and ZSwP, which was highly negative and therefore signiﬁcant in the 40 – 49 and 50 – 69-day-old groups, was not remarkable in the 70 –107-dayold group. Similarly, SwNSw and ZSwP correlated to a signiﬁcant degree only in the third group. However, the relationship between these two angles was of a positive nature. NcEcEn, SwNSw, and SwPSw correlated highly negatively with each other, as did NcEcEn with ZPZ. This situation was observed only in the 50 – 69-day-old group. The correlation of NcEcEn with AZP in the same group was still noteworthy, but this time it was highly positive. Category 4 In this category, the examination of the correlations between the angles and skull index revealed that the degree of the angles decreased with age. The only signiﬁcant and highly negative correlation of the skull index was with AZP in the 40 – 49-day-old group. However, in the group of 50 – 69-day-old puppies, the skull index was noted to have important and highly positive correlations with ZAZ, ZNZ, ZPZ, NcPNc, and SwPSw. Another remarkable, though positive, correlation of the index in the same group was with AZP and AZN. In the third group (70 –107-day-old puppies), the index continued to correlate highly negatively with AZP but positively with ZPZ. However, its correlation with AZN, which was highly negative in the second group (50 – 69day-old puppies), was not observed in the third group. In all three groups, the index correlated highly positively with NcNNc, SwNSw, ZSwP, ZSwN, and ZswEn, and negatively with ANcBr, ANcN, AncP, and NSwP. DISCUSSION Dog breeds present a spectacular intraspeciﬁc polymorphism. The shape and morphometry of dog skulls are therefore important parameters for determining morphological types. Researchers can examine geometric morphometries to determine the skull forms of adult dogs, as well as to assess changes in shape that occur during development. By taking an ontogenetic approach, investigators can observe these shape changes until the formation of the adult skull is complete. During this period of time, angular measurements made on skulls can play a significant role in the appraisal of growth processes. It was observed in our study that German shepherd puppies start out in life with a wide, circular neurocra- 465 nium. It was also noted that some morphological changes in their skulls, such as the manifestation of the external sagittal crest and external occipital protuberance, occur between birth and maturity. These changes in shape resulted in a decrease of the skull index. The high skull index in the group of 40 – 49-day-old puppies was due to a wider maximum zygomatic width compared to the total skull length. However, as the puppies grew older, the former value did not increase in proportion to that of the total skull length, which explained the decrease in the skull index. Subsequently, the lowest skull index was observed in the 70 –107-day-old group. Although these skull indices were greater than those in dolichocephalic breeds (Evans, 1993), it was ascertained that they tended to decrease as the puppies grew older. This indicated that the puppy skulls developed longitudinally. The angular measurements and their relationships to each other correlated with the fact that the noses of German shepherds become longer as the dogs develop. The geometrical analysis based on the zygion points (Fig. 1a and b) revealed that the increase in the zygomatic width, which was in proportion to age, was less than that of the skull length. On the other hand, the decrease in ZAZ, ZPZ, and ZNZ with age, and their highly positive and signiﬁcant correlation with the skull index, made it clear that the skull length increased more compared to its width. This demonstrated that the shape of the skull shifted to that of a narrow, long one. In support of this observation, the AZP and AZN angles extended as the puppies grew older. A geometrical analysis based on both the left and right euryon points (Fig. 2a and b) showed that the degrees of the angles of NcANc, NcPNc, NcNNc, and NcBrNc declined with age, and that the skull index correlated highly positively and signiﬁcantly with NcPNc and NcNNc. This resulted in the neurocranium having a narrow, long appearance in line with the lengthened skull. That the angle degree of NcBrNc narrowed with age indicated that the bregma point proceeded forward as a result of the altered appearance (narrower and longer) of the neurocranium. When the geometrical shape drawn by joining the narrowest lateral points of the nose was analysed (Fig. 3a and b), it was noted that as a result of the decrease in SwNSw and SwPSw with age, the degree of NSwP widened, which resulted in the viscerocranium having a narrow, long shape, both orally and aborally. Furthermore, the highly positive correlation between the skull index and SwNSw and SwPSw, which showed that the increase in skull length was greater than that of the zygomatic width, was another indicator that the viscerocranium developed lengthwise and narrowed as it did so. So far, the skull base has been the only point of origin for examinations of alterations in skull shape. A biometrical analysis of curvatures in the skull base of adult dogs has been performed (Nussbaumer, 1985), and variations in the length of the palatine bone with age have also been shown in newborn puppies (Nussbaumer, 1978). However, the changes that occur in the skulls of puppies have not been studied as a whole. Data obtained from both the dorsal and ventral crania play a part in investigations of the growth processes that occur in the skull. The development of the basiocranium, in particular, has a great inﬂuence on the overall growth trajectories of the neurocranium. However, in this study we have only discussed changes in the geometrical morphometry of the dorsal crania. It has been reported that 466 ONAR AND GÜNEŞ changes in the morphology of the dorsal crania may have an effect on craniofacial development (Onar, 1999). Therefore, we believe that the observed angular changes in the dorsal crania may in part explain the changes that occur in the shape of the dog skull during growth. In our previous study (Onar, 1999), a morphometric analysis of the skull of German shepherd dogs, which is a dolichocephalic breed, was made, and the changes with age of the craniometric measurements were given in detail. Below are the ﬁndings that suggest that the skulls of German shepherd puppies will have a dolichocephalic appearance and become narrower and longer as the puppies reach adulthood: Geometrical variations in the shape of the skull occur during the dolichocephalic development of German shepherd puppies, as indicated by angle measurements. German shepherd puppies have a wide, circular neurocranium. Previous morphometric evaluations support the notion that the development of the skull of a German shepherd puppy is of a dolichocephalic nature (Onar, 1999). We hope this study will be of some assistance to those who may wish to examine the ventral crania and the development of the skull as a whole. ACKNOWLEDGMENT The authors thank Mr. Cüneyt Bademcioğlu for his invaluable contribution to the translation of this article. LITERATURE CITED Brehm H-V, Loefﬂer K, Komeyli H. 1985. Skull shape in the dog. Anat Histol Embryol 14:324 –331. Evans HE. 1993. The skeleton. In: Evans HE, editor. Miller’s anatomy of the dog. 3rd ed. Philadelphia: W.B. Saunders Co. p 122–166. Evrim M, Güneş H. 1998. Biometry. Istanbul: Istanbul University Veterinary Fac. Press. p 1–58. Hidaka S, Matsumoto M, Hiji H, Ohsaka S, Nishinakawa H. 1998. Morphology and morphometry of skulls of raccoon dogs, Nyctereutes procyonoides, and badgers, Meles meles. 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