Morphometric Study of Mus musculus, Rattus norvegicus, and Rattus rattus in Qatar

Simple Summary Rodents are the most abundant and diversified group of mammals. These animals show genetic and physical diversity in different ecosystems of the world, including the desert ecosystem. The current study was undertaken to check the morphometric pattern of three commensal rodent species, viz, Mus musculus, Rattus norvegicus, and Rattus rattus, in Qatar. One hundred forty-eight rodents were captured and studied for body and cranio-mandibular measurements. The study found R. norvregicus as the most prevalent rodent in Qatar. Most of the rodents were collected from Al Rayan municipality, were adults, and were from livestock farms. The rodents’ average body weights were 18.8 ± 2.2 gm, 264.3 ± 87.5 gm, and 130 ± 71.3 gm for M. musculus, R. norvegicus, and R. rattus, respectively. The average morphometric measurements of the external body and skull were normally distributed and can be used as a reference of R. norvegicus and R. rattus for Qatar. Abstract The current study was undertaken to estimate the morphometric pattern of three commensal rodents, i.e., Mus musculus, Rattus norvegicus, and Rattus rattus in Qatar. One hundred forty-eight rodents were captured from different facilities throughout Qatar. The captured rodents were used to identify the external body and cranio-mandibular morphometry. The study found that R. norvregicus was the most prevalent (n = 120, 81%, 95% CI: 73.83–87.05). Most of the rodents were collected from Al Rayan municipality (n = 92, 62%), were adults (n = 138, 93.2%, 95% CI: 87.92–96.71), and were from livestock farms (n = 79, 49%, 95% CI: 41.02–57.65). The rodents’ average body weights were 18.8 ± 2.2 gm, 264.3 ± 87.5 gm, and 130 ± 71.3 gm for M. musculus, R. norvegicus, and R. rattus, respectively. The research found that the studied rodents are smaller than those of other countries such as Turkey, Tunisia, and Iran. The study of morphometry is a useful tool for the traditional identification of small mammal species, including rodents. The average morphometric measurements of the external body and skull were normally distributed and can be used as a reference of R. norvegicus and R. rattus for Qatar. A further comprehensive study is required to investigate the rodent population index, eco-friendly control program, and public health importance in Qatar.

Single rodent traps (SRT) and 100 multi rodent traps (MRT). We used different baits such as bread (Arabian khubj), biscuits, potato chip, and cheese for captu rodents [22]. An SRT or MRT was used randomly, without targeting any specific species or the species behavior. A water bottle containing 5% glucose was affixed trap to reduce dehydration and stress of the captured animals in the harsh Qata ronment. The trappings covered six facilities: family residents, bachelor residen cultural farms, livestock farms, industrial areas, and commercial areas throughou ( Figure 1). The traps were set for a single night. Successful traps were collected morning and transferred at the earliest convenience to the veterinary laboratory Qatar. A comfortable temperature was maintained (20-25 °C) in the transporta and veterinary laboratory rodent room. The traps were washed with soap and pres water and air-dried to avoid any residual contamination and transmission from vious rodent to the next.

Rodent Identification and Morphometric Assessment
The captured rodents were euthanized using 5% isoflurane inhalation for five minutes in a desiccator. After weighing with an electronic balance (Serial No. 057700082, Kern EG420-3NM, Kern & Sohn GmBH, Balingen, Germany), morphological appearance and external measurements were recorded as per species, age, sex, and pregnancy [22][23][24][25]. Rodent species were identified based on morphologic characteristics and measurements. The animals were assessed for sex (female or male) using external and internal aspects of reproductive organs such as testicles, penis, seminal vesicles, vagina, mammary teats, and possible pregnancy signs. For age detection, we only identified the adult rodents. Developed genital organs and pregnancy were the sign of an adult rodent. Additionally, we considered prominent temporal ridges and postorbital processes of the skull to determine a rodent as mature. The presence of a gravid uterus served as the indicator of pregnancy.
Five standard external measurements were made for the animals using a ruler ( Figure 2). Following the morphological characterization, the rodents were dissected, skulls were collected, cleaned, and dried according to the standard procedure [26]. The cranium and mandible morphometric variables were recorded using a digital caliper (TESA TWIN-CAL IP67, Hexagon, Switzerland) described previously [9,[27][28][29] and illustrated in  Animals 2021, 11, x 4 of 15

Rodent Identification and Morphometric Assessment
The captured rodents were euthanized using 5% isoflurane inhalation for five minutes in a desiccator. After weighing with an electronic balance (Serial No. 057700082, Kern EG420-3NM, Kern & Sohn GmBH, Balingen, Germany), morphological appearance and external measurements were recorded as per species, age, sex, and pregnancy [22][23][24][25]. Rodent species were identified based on morphologic characteristics and measurements. The animals were assessed for sex (female or male) using external and internal aspects of reproductive organs such as testicles, penis, seminal vesicles, vagina, mammary teats, and possible pregnancy signs. For age detection, we only identified the adult rodents. Developed genital organs and pregnancy were the sign of an adult rodent. Additionally, we considered prominent temporal ridges and postorbital processes of the skull to determine a rodent as mature. The presence of a gravid uterus served as the indicator of pregnancy.
Five standard external measurements were made for the animals using a ruler ( Figure 2). Following the morphological characterization, the rodents were dissected, skulls were collected, cleaned, and dried according to the standard procedure [26]. The cranium and mandible morphometric variables were recorded using a digital caliper (TESA TWIN-CAL IP67, Hexagon, Switzerland) described previously [9,[27][28][29] and illustrated in Figures 3-6.

Rodent Identification and Morphometric Assessment
The captured rodents were euthanized using 5% isoflurane inhalation for five minutes in a desiccator. After weighing with an electronic balance (Serial No. 057700082, Kern EG420-3NM, Kern & Sohn GmBH, Balingen, Germany), morphological appearance and external measurements were recorded as per species, age, sex, and pregnancy [22][23][24][25]. Rodent species were identified based on morphologic characteristics and measurements. The animals were assessed for sex (female or male) using external and internal aspects of reproductive organs such as testicles, penis, seminal vesicles, vagina, mammary teats, and possible pregnancy signs. For age detection, we only identified the adult rodents. Developed genital organs and pregnancy were the sign of an adult rodent. Additionally, we considered prominent temporal ridges and postorbital processes of the skull to determine a rodent as mature. The presence of a gravid uterus served as the indicator of pregnancy.
Five standard external measurements were made for the animals using a ruler ( Figure 2). Following the morphological characterization, the rodents were dissected, skulls were collected, cleaned, and dried according to the standard procedure [26]. The cranium and mandible morphometric variables were recorded using a digital caliper (TESA TWIN-CAL IP67, Hexagon, Switzerland) described previously [9,[27][28][29] and illustrated in Figures 3-6.

Statistical Analysis
The data were analyzed using statistical software StatSoft (2011) to study the descriptive analysis of the number of captured rodents and their morphometric variables that included mean, percentage (%), 95% confidence interval (CI), standard deviation (SD), skewness, standard error of skewness, kurtosis, and standard error of kurtosis. The data were tested with the Kolmogorov-Smirnov test, skewness, and kurtosis to validate the normality. If the skewness and kurtosis were outside −2 and +2, the measurement was considered significantly skewed or kurt [30,31]. The student t-test was performed to examine the variability of the morphometric traits among sex (female vs. male) and pregnancy (pregnant vs. non-pregnant). The chi-square (χ 2 ) test was performed to examine the level of significance (p < 0.05) among the area (municipality) and trapping location types.
Animals 2021, 11, x 6 of 15 Figure 6. Lateral view of rodent mandible with linear measurements and identification marks. Length of lower incisor (a to b), Distance between lower incisor to coronoid process (a to g), Distance between lower incisor to condyloid process (a to f), Distance between lower incisor to angular process (a to e), Greatest jaw height (GJH) (d to g), Ramus to Molar tooth 1 (c to j), Distance between lower molar tooth 1 to molar tooth 3 (h to i), and Distance between lower incisor to molar tooth 1 (a to i).

Statistical Analysis
The data were analyzed using statistical software StatSoft (2011) to study the descriptive analysis of the number of captured rodents and their morphometric variables that included mean, percentage (%), 95% confidence interval (CI), standard deviation (SD), skewness, standard error of skewness, kurtosis, and standard error of kurtosis. The data were tested with the Kolmogorov-Smirnov test, skewness, and kurtosis to validate the normality. If the skewness and kurtosis were outside −2 and +2, the measurement was considered significantly skewed or kurt [30,31]. The student t-test was performed to examine the variability of the morphometric traits among sex (female vs. male) and pregnancy (pregnant vs. non-pregnant). The chi-square (χ 2 ) test was performed to examine the level of significance (p < 0.05) among the area (municipality) and trapping location types.

Demographic Information
The study captured 148 rodents from all seven municipalities of Qatar (Table 1, Figure 1). A total of 79 rodents were captured by SRT and 69 rodents by MRT. The thirty-two MRT captured more than one rodent (2-5) at a time. Based on the morphologic and morphometric characters of the body and skull, three species of rodents were identified, i.e., M. musculus, R. rattus, and R. norvegicus. R. norvegicus comprised 81.1% (n = 120) of the total captured rodents, whereas R. rattus (n = 24) and M. musculus (n = 4) showed low density. Most of the collected rodents (n = 138, 93.2%) were adults. A major portion of the captured rodents was collected from Al Rayan municipality (n = 92, 62%). This municipality harbors all the three commensal species (M. musculus and R. rattus, and R. norvegicus), showing (χ 2 = 21.02, p < 0.05) the highest density for R. norvegicus (n = 64). The majority of the rodents (n = 79, 49%) (χ 2 = 35.29, p < 0.05) were collected from the livestock farms.  , Distance between lower incisor to coronoid process (a to g), Distance between lower incisor to condyloid process (a to f), Distance between lower incisor to angular process (a to e), Greatest jaw height (GJH) (d to g), Ramus to Molar tooth 1 (c to j), Distance between lower molar tooth 1 to molar tooth 3 (h to i), and Distance between lower incisor to molar tooth 1 (a to i).

Demographic Information
The study captured 148 rodents from all seven municipalities of Qatar (Table 1, Figure 1). A total of 79 rodents were captured by SRT and 69 rodents by MRT. The thirtytwo MRT captured more than one rodent (2-5) at a time. Based on the morphologic and morphometric characters of the body and skull, three species of rodents were identified, i.e., M. musculus, R. rattus, and R. norvegicus. R. norvegicus comprised 81.1% (n = 120) of the total captured rodents, whereas R. rattus (n = 24) and M. musculus (n = 4) showed low density. Most of the collected rodents (n = 138, 93.2%) were adults. A major portion of the captured rodents was collected from Al Rayan municipality (n = 92, 62%). This municipality harbors all the three commensal species (M. musculus and R. rattus, and R. norvegicus), showing (χ 2 = 21.02, p < 0.05) the highest density for R. norvegicus (n = 64). The majority of the rodents (n = 79, 49%) (χ 2 = 35.29, p < 0.05) were collected from the livestock farms.

Morphometric Assessments of Rodents
The overall means of body weight, external morphometry, and cranio-mandibular variables per species are presented in Tables 2-4. Out of the 148 rodents, 108 rodents were dissected, comprised of 86 R. norvegicus, 18 R. rattus, and 4 M. musculus. The average body weight was variable among three rodent species (18.8 ± 2.2 gm, 264.3 ± 87.5 gm, and 130 ± 71.3 gm for M. musculus, R. norvegicus, and R. rattus, respectively). The skewness and kurtosis statistics of all the studied external body measurements of R. norvegicus and R. rattus were within −2 and +2. This indicated that the observed values were normally distributed. In general, the tail is longer than the length of the body and head of M. musculus and R. rattus, which is the opposite in R. norvegicus. Compared to the general length of a rodent, the ears and legs of R. rattus are longer than that of R. norvegicus. As the captured number of M. musculus was small, no further statistical comparative analysis could be considered on their body or cranio-mandibular measurements.  Table 3. Cranial morphometric linear measurements (mean ± SD) of the commensal rodents of Qatar.  The t-test showed that there is no sexual or pregnancy-related dimorphism (p > 0.05) in any of the presented characteristics in the case of R. norvegicus (Tables 5-10). However, the right ear length measurements showed that females have longer ears than males in R. rattus. Moreover, the mandibular characters, such as the length of lower incisors and the distance between lower incisor to coronoid process, lower incisor to condyloid process, lower incisor to angular process, ramus to molar tooth 1, and lower incisor to molar tooth 1 of R. rattus, were significantly higher in females than males (p < 0.05). In addition, the value of lower molar tooth 1 to molar tooth 3 was higher in the case of males than females in R. rattus (Table 7). Furthermore, the right hind leg was longer (p > 0.05) in non-pregnant than pregnant R. rattus (Table 8).         Table 10. Pregnancy-related mandibular morphometric dimorphism (mean ± SD) in Rattus norvegicus and Rattus rattus.

Rattus norvegicus Rattus rattus
Our study revealed that most of the rodents were from livestock farms. The livestock farms are mostly made up of mixed livestock species with poor management and biosecurity [35], making an ideal place for rodents to colonize and why we captured a major part of rodents from these places. A previous study reported that over 75% of the livestock farms were infested with rodents, mainly by R. norvegicus, and the incidence of house mouse M. musculus was detected less in Qatar [13], which is congruent with the present study. Out of the 148 captured rodents, only four were M. musculus.
Traditional morphometry is a valuable tool for species identification in small mammals, including rodents [28,36]. The present study found the body weight and general body length of R. norvegicus as 264.3 gm and 398.5 mm, respectively, which were 259 ± 85.2 gm and 405 ± 54.7 mm, respectively, for the same species in Turkey [37]. In the case of cranial morphometry, the condylobasal length and the zygomatic breadth of R. norvegicus in the current study were 45.2 mm and 22.4 mm, which were 45.52 mm and 23.75 mm in the case of Turkey [37] and 46.84 mm and 21.64 mm in the case of Iran [38], respectively, for the same species and measurements. The overall body length of R. rattus in Turkey was 378.43, which was 324.4 mm for the same species of Qatar. The cranial length and zygomatic width of R. rattus in the current study were 37.2 mm and 18.2 mm, which were 39.15 mm and 19.86 mm, respectively, for Turkey [37] and 39.08 mm and 19.97 mm, respectively, for Tunisia, respectively for the same species and measurements [39].
Similarly, the body length of M. musculus in Qatar was 78.5 mm, which was 85.41 mm [24] and 88.0 mm [40] for the same species from different parts of Iran. Due to the small sample size (n = 4), we do not have strong support in the results of M. musculus morphometry. However, the overall body and cranial size indicate that the three studied rodent species in Qatar are comparatively smaller than the same species from the countries like Turkey, Tunisia, and Iran. This variation may be due to Qatar harsh environmental effects [6][7][8], which is supported by Bergmann's rule [41]. Rodents of the colder environment are bigger in body size than the wormer environment [42,43]. This further highlights the necessity of performing traditional morphometry on the geographic population of rodents, specifically cosmopolitan species.
Based on the average general body and skull morphometric measurements, males were slightly larger than females, although there is no significant sexual dimorphism. This finding is supported by a previous study by Ventura and Lopez-Fuster [7]. However, the present study showed that the body and cranio-mandibular linear measurements of commensal rodents in Qatar were normally distributed for the two species, R. norvegicus, and R. rattus. Bodyweight and body and skull linear measurements distribution shape were approximately symmetric since the statistic of skewness measures were between −0.2 and 0.2 [30,31]. Normality analysis of the biometric traits can be considered typical characteristics of the two rodent species, R. norvegicus and R. rattus, in this country. To the best of the authors' knowledge, such work is the first time in Qatar. Therefore, the current study can be used as a reference for morphometric measurements of the commensal rodents in this country, especially for R. norvegicus and R. rattus.

Conclusions
The current study estimated, identified, and characterized the morphometric variables of three commensal rodents in Qatar. The research identified that the commensal rodents of Qatar are comparatively smaller than the same species of some other countries, such as Iran, Tunisia, and Turkey. The is the first study on rodent morphometry in Qatar and even in the Arabian Peninsula. Due to geo-ecological similarities, the present study can be a reference study to rodent or small mammal identification in Qatar and other countries of the Arabian Peninsula.