Morphological Variations in the Skulls of Male and Female Persian Fallow Deer (Dama dama mesopotamica)

Introduction

Persian fallow deer (PFD) with the scientific name Dama dama mesopotamica, as one of the rarest deer species in the world, was previously abundant throughout western Asia. Nowadays, they are inhabiting only a small habitat in Khuzestan, Southern Iran, two rather small protected areas in Mazandaran Province (Northern Iran), and some other small areas in the Near and Middle East. This member of the subfamily Cervinae belonging to the family Cervidae is currently listed as endangered by the International Union for Conservation of Nature (Jantschke, 1990; Rabiei and Saltz, 2011; Berger-Tal et al., 2012; Ekrami et al., 2016; Vigne et al., 2016).

Due to the importance of skull anatomy in diverse fields of science, including clinical and surgical practices, wildlife and evolutionary sciences, and sexual dimorphism. Therefore, many studies have been carried out on distinct animals, such as various species of dogs, equines, felines, porcine, sheep, talpas, and rodents (Kieser and Groeneveld, 1992; Evans and McGreevy, 2006; Carreira and Ferreira, 2016; Pitakarnnop et al., 2017; Kyllar et al., 2016; Choudhary and Singh, 2016; de la Barra et al., 2020; Selçuk et al., 2019; Selçuk et al., 2018). Marzban Abbasabadi et al. (2018) evaluated the morphometric differences of the skull between male and female Zell sheep. They found significant in sexual dimorphism between males and females. Parés‐Casanova (2015) analyzed the skulls of adult White Rasquera goat breed to explore sexual dimorph-ism based on geometric morphometric in this local goat breed. Their results demonstrated that the differences in the skull of the two genders may be attributed to the extensive management styles of the animals as under a low anthropogenic influence they tend to reinforce their natural sexual size dimorphism.

In this regard, some studies have evaluated skull anatomy in various species of the Cervidae family. Markov (2014) analyzed the extent of sexual dimorphism in the skull features of red deer (Cervus elaphus L.) in Bulgaria and reviewed the population morphometric variations in the skull of red deer from mountainous and lowland habitats. In addition, there are many studies on skull anatomy in European roe deer (And and Reig, 1993; Sabalinkiene et al., 2017). However, information about PFD skull anatomy is limited. Therefore, the current study aimed to evaluate morphological differences in the skulls of male and female PFDs.

Materials and Methods

Samples Preparation

In cooperation with the Department of Environment of Mazandaran province, Iran, a total of nine PFD skulls or heads (five adult male and four adult female) were obtained from the museum of the Department of Environment and the dead deer of Dasht-e Naz Wildlife Refuge, Sari, Iran protected area during the past two years. Only the skulls of adult PFDs with completely formed dentition were used (Selçuk et al., 2018). The heads and skulls were examined for any skeletal damages or deformities and then the heads were prepared by boiling method. Next, the mandibles were disarticulated from the temporomandibular joint. The samples were numbered and photographed (Canon EOS 4000D, Tokyo, Japan) from dorsal, lateral, ventral, and caudal views. During photography, the camera and the samples were fixed in place to keep the distance and angles of the shots constant.

Morphological Observations

At the first step, the male and female PFD skulls and mandibles were assessed to find remarkable morphological differences. As the horns or cornual process are different between sexes, the other components of the skull and mandible were searched. Afterwards, the accuracy of the found hallmarks was examined.

Morphometric Geometric Studies

As demonstrated in Figures 1 and 2, ten, six, and nine landmark points were defined on the left lateral photos of mandibles and the dorsal and left lateral photos of skulls, respectively. These points were digitized on two-dimensional (2D) images using the TpsDig2 software version 2.16 (Rohlf, 2010).

The adequacy of tangent shape for statistical analysis was investigated utilizing the TpsSmall (Rohlf, 2003). The non-shape inform-ation was removed from landmark configurations applying General Procrustes Ana-lysis The covariance matrices were generated and the shape differences between the two sexes were analyzed by the discriminant function analysis (DFA) in the MorphoJ version 1.02j (Klingenberg, 2011). The patterns of skull and mandible shape differences were illustrated in the wireframe relative to each other for quantification and visualization purposes.

Morphometric Measurements

For morphometric measurements, 11 parameters in the mandibles and 18 parameters in the skulls selected based on the previous studies (Figures 3 and 4, Tables 1 and 2) were calculated utilizing digital Vernier caliper (Digimatic Caliper, Japan) with an accuracy of 0.01 mm. All measurements and observations were blinded (Pitakarnnop et al., 2017; Onuk et al., 2013). Data were analyzed by the independent samples t-test using the SPSS software version 16 (SPSS Inc., Chicago, USA). The level of significance was considered as P-value

Figure 3. Measured parameters in lateral view (A), medial view (B) and dorsal view (C) of the mandible of Persian fallow deer (Dama Dama Mesopotamica): (A) Condyloid fossa to height of mandible (TMA), Condyloid fossa to base of mandible (MMA), Maximum height of mandible (MH), Total length of mandible (ML), Mental foramen to first premolar (MM), Lateral alveolar root to mental foramen (MI), Length of diastema (DL). (B), Caudal border of mandible to beneath of mandibular foramen (CBM), Mandibular foramen to the caudal border of mandible (CM), Mandibular foramen to base of mandible (MB). (C), The interior angle between the bodies of the mandible (Angle)

Table 1. Description of 11 measurements taken from the mandible (see details in Figure 3).

Figure 4. Measured parameters in dorsal view (A), lateral view (B) and ventral view (C) of the skull of Persian fallow deer (Dama Dama Mesopotamica): (A), NCB. Neurocranium breadth; TB. Total breadth; DS. distance between two supraorbital foramens; NL. Nasal length. (B), TL. Total length; CBL. Condylobasal length; UTL. Upper tooth row length; MCI. Medial canthus to infraorbital foramen; RL. Rostrum length; MCI. Medial canthus to infraorbital foramen; MCS. Medial canthus to supraorbital foramen; OH. Orbital height; OW. Orbital width. (C), ZIB. Zygomatic breadth; BL. Basal length; FMH. Foramen magnum height; FMW. Foramen magnum width.

Table 2.Description of 18 measurements taken from the skull (see details in Figure 4).

Results

Descriptive Anatomy of Male and Female Persian Fallow Deer

As our observations revealed, the interfrontal ridge was prominent in male PFD and flat in female PFD (accuracy rate: 90.47%). In addition, the dorsal surface of the frontal bone was concave in females and flat and more extended in males (accuracy rate: 85.71%) (Figure 5).

Morphometric Geometric Results

According to the DFA performed in this study, there was no significant sexual dimorphism in the skull of PFD. However, in some defined landmarks, some differences were observed between sexes, which were somewhat consistent with the findings of morphometric studies (Figure 6).

Morphometric Measurements

Results of the descriptive analysis are presented in Tables 3 and 4. The results showed significant differences in some measured parameters of the skull and mandible of male and female PFDs. The total breadth of the skull, upper tooth row length, temporalis muscle moment arm, diastema length, mental foramen distance to P1 and I4, and mandible total height were significantly larger in male PFDs, compared to female animals. However, the distance between the mandibular foramen and the caudal border of mandible angle was significantly higher in female PFDs than in male cases (Tables 3 and 4).

 Figure 5. Dorsal view of the skulls of the male (A) and female (B) Persian fallow deer (Dama Dama Mesopotamica), showing the more prominent interfrontal ridge in male PFD (red oval) (A) (accuracy rate= 90.47%).

Table 3.Morphometric data of Persian fallow deer (PFD) skull in mm (M±SE).

^a,b Values within a row with different superscripts differ significantly at P<0.05

Table 4.Morphometric data of Persian fallow deer (PFD) mandible in mm (M±SE).

^a,b,c,d,e,f Values within a row with different superscripts differ significantly at P<0.05

Discussion

Due to the importance of skull anatomy (Alsafy et al., 2014; de la Barra et al., 2014; Farhadinia et al., 2014; Samuel et al., 2016; Parés‐Casanova and Fabre, 2013; Moham-madpour, 2011), morphological variations in the skulls of male and female PFDs were evaluated in this investigation. Descriptive morphological examinations of male and female skulls demonstrated more prominent interfrontal ridge and flatter frontal bone in males, compared to female subjects. There is no published study revealing hallmarks between male and female PFDs. However, it was expected to find differences in the bony structures of this area between sexes because of the pressure of horn growth on the frontal zone (Pėtelis and Brazaitis, 2003).

According to the morphometric-geometric results of this study, male and female PFDs were not significantly different in terms of the defined landmarks of the skulls and mandibles. However, some differences were observed in the caudal curvature of the mandible and some parameters defined in the facial part of the skull lateral view. The latter differences were somewhat consistent with the morphometric results. Based on the morphometric results, five parameters of the mandible, including the distance between mental foramen to the first premolar and forth incisor tooth (MM and MI), length of diastema (DL), Total height of mandible (MH), and the length of temporalis muscle moment arm (TMA), as well as two parameters in the skull, namely the total breadth (TB) and upper tooth row length (UTL), were significantly larger in males than females. Furthermore, the CBM was significantly larger in female PFDs than the male cases.

It was shown that the mandible is a more accurate bone for distinguishing the skulls of male and female PFDs. Reig (1993) compared the craniometrics variability between two roe deer populations in Spain. They reported the mandible to be the most variable trait with significant differences between populations. Marzban Abbasabadi et al. (2018) surveyed morphometric differences of the skull in male and female Zell sheep and observed the only significant difference in mandible. Their findings indicated that the distance of lateral alveolar root to mental foramen was significantly higher in male Zell sheep than in females. In addition, in studies on skull dimorphism on other animals, such as the Feline (Felis catus) species, the only significant morphometric difference of skull was observed in the mandible where the masseteric moment arm (MMA) was higher in males than female animals (Pitakarnnop et al., 2017).

In the Cervidae family, some studies have used skull or other parts of the skeleton to find the distribution of the subspecies, differentiate between populations, and assess the colorations with age, body mass, and some other variables. Most such studies have been performed on roe deer to examine morphometric differences. In some of these investigations, the diversity of the craniometrics parameters was large enough to divide the population into different groups or ecotypes. Blagojević and Milošević-Zlatanović (2011) evaluated sexual shape dimorphism in Serbian roe deer (Capreolus capreolus L.) by combining the multi-variate statistical procedures with geometric morphometrics and visualization techniques. These authors reported distinct patterns of shape variability in male and female animals as the cranial base was broader in males, while elongated and slenderer-shape with narrower basicranium in female skulls.

Sabalinkiene et al. (2017) revealed that geographical location has a significant effect on the antler morphometry traits and skull size of male roe deer. Furthermore, they reported the impact of gender on the skull morphology traits at juvenile age. Based on their results for the zygomatic arch internal breadth (ZIB), the influence of gender was equally important in all age classes, whereas for ML, UTL, NL, the gender effect was stronger at the juvenile stage than at the mature stage. Concerning DL, age had a relatively stronger effect at the mature stage. They revealed that males showed higher measurement values in almost all measured traits in all age classes.

Kim et al. (2013) detected the sexual dimorphism of the Korean water deer in cranial trait by the size of TL, CBL, and BL, which were similar to our results. However, they reported that the skull size of female subjects was larger than that of male animals, which is a unique pattern among mammals. According to the previous studies, the UTL, ZIB, DL, and TB of the skull were the most common parameters that showed significant differences between genders or populations. The findings concerning TB, UTL, and DL are in line with the present study (And and Reig, 1993; Aragon et al., 1998; Pėtelis and Brazaitis, 2003; Shereme-tyeva and Sheremetyev, 2008; Sabalinkiene et al., 2017).

Conclusion

This investigation revealed some morphological differences between the skulls of male and female PFDs. Moreover, measured parameters in the morphometric studies, similar to other investigated members of the Cervidae family, showed a significant difference between genders. The latter result might reveal the significant role of these parameters in gender detection.

Acknowledgments

This research work has been supported by a research grant from Amol University of Special Modern Technologies, Amol, Iran. The authors would like to thank Department of Envir-onment of Mazandaran Province, Mazandaran, Iran, for great helping in collecting the specimens.

Conflict of Interest

The authors declared that there is no conflict of interest.