EurAsian Journal of BioSciences Eurasia J Biosci 14, 6657-6663 (2020)

Histomorphological study of the male genital system in the long eared Hemiechinus aurtus

Ammar Ismail Jabbar 1*, Ramzi Abdulghafoor Abood Al-Agele 1, Ahmed Abdulla Hussein Al Ubaidy 1 1 Department of Anatomy and Histology, College of Veterinary Medicine, University of Diyala, IRAQ *Corresponding author: [email protected]

Abstract The current study was aimed to cover the gross and histological structures of the in the long eared hedgehog Hemiechinus aurtus. Eight male were used in this study. Anatomically, the male long eared hedgehog had two intra-abdominal testis and had a clear urethral process and sigmoid flexures with two ribbon of retractor muscle directed cranially that was similar to that of fibrous type penis. The possessed two nail like structure similar to that of insectivores. The accessory sex glands were recognized by the massive size of the seminal vesicle that was extended to reach to the abdominal cavity with the average length was 30.24±1.76 mm and width 34.75± 2.03mm. Similarly, were also showed large size with the average length 21.95± 0.49 mm and width 29.29± 0.72 mm. While, showed lesser size with the average length 13.91±0.67 mm and width 14.77±0.31 mm. However, it was observed the absent of the ampulla ductus deference gland that was different from that in other Insectivora. The histological observations illustrated that the male genital system of long eared hedgehog were at sexual activity and they follows the mammalian pattern.

Keywords: long eared hedgehog, penis, testis, accessory genital glands

Jabbar AI, Al-Agele RAA, Al Ubaidy AAH (2020) Histomorphological study of the male genital system in the long eared hedgehog Hemiechinus aurtus. Eurasia J Biosci 14: 6657-6663.

© 2020 Jabbar et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License.

INTRODUCTION in the literature about the genital glands in hedgehog. Therefore, the current research was intended to exam belong to the family , order the macro and micro structures of male genital system Insectivora include several species and genuses and accessory sex glands in long eared hedgehogs and (Corbet, 1988; Reiter and Gould, 1988). The (native to contribute to the knowledge of this field. species) Iraqi hedgehog is under the long ear hedgehog Hemiechinus aurtus (Çolak et al. 1988; Hutterer, 2005). MATERIALS AND METHODS Hedgehog is considered beneficial because it eats many harmful insects, including termites and even scorpions Sample collection (Roberts, 1977). The male reproductive system consists A total of eight adults healthy male long-eared of the organs that are participated in the development, hedgehog (Hemiechinus auritus), were captivated from maturation, transport and deposition of the male semen. the Diyala fields from period of time April to May (season It includes a paired testis, , ductus deference, of reproduction) with average body weight (216.5± 13.78 and penis and accessory genital glands (Konig et al. gm) (Table 1) (Fig. 1). This study was conducted under 2009). The accessory sex gland consists of seminal the order no. 310/ H. S. of the Ethic Committee of the vesicle, ampulla ductus deference, prostate, Council of the Veterinary Medicine College/ Diyala bulbourethral and urethral glands, their presence varies University. among the species and may be include all or some The body weights were recorded then the (Konig et al. 2009). Even so not all structures are present hedgehogs euthanized with high dose of ketamine 30 in all mammalian order (Konig et al. 2009). While there mg/ kg and xylazine 5mg/ kg body weight via are some studies on the male reproductive system in intramuscular injection. The ventral surface of the wild carnivores and insectivores, (Contreras and Bustos- abdomen and inguinal region was photographed before Obregón, 1980; Collins et al. 1982; Hijikata et al. 1986; skinned to show the morphology of penis, after that, the Beguelini et al. 2013; Danmaigoro et al, 2014; Akbari and Davoud, 2017; Fard and Farangis 2017), very little Received: November 2019 Accepted: March 2020 was found concerning the reproductive system in male Printed: December 2020 Iraqi hedgehog. Furthermore, there are no practical data

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Table 1. Biometric data shows mean body weight, gross measurements of various parts of reproductive tract in hedgehog (n=8) Length(mm) Width(mm) Thickness(mm Circumferane weight (gm.) left 20.14± 0.39 11.29±0.43 9.76±0.18 40.11± 0.17 1.15±0.10 Testis right 19.05± 0.46 10.87±0.68 10.08±0.94 40.03±0.37 1.13±0.02 left 38.32±0.31 - - - Epidydmis right 38.09±0.28 - - - penis 36.6±2.15 7±0.6 (DV) 6.5±0.37( LL) - Seminal vesicle. 30.24±1.76 34.75± 2.03 9.038± 1.15 - 5.06±0.17 Prostate 21.95± 0.49 29.29± 0.72 7.18± 0.45 - 2.64±0.13 left 14.77±0.31 13.91±0.67 6.07±0.42 - 1.20±0.07 Bulbourethral right 14.81±0.32 14±1.03 6.37±0.65 - 1.16±0.05

calibrated using a Fiji J software. These measurements were performed on each photomicrograph and the data were recorded as mean ± SDM.

RESULTS Anatomical features The reproductive system of the male hedgehog was found to have paired testis, epididymis, dudctus deference, penis and accessory genital glands. The testes were oval in shape, creamy in color, and located intra-abdominal. The two testes appear as a paired bulges emerging from under the skin of both side of the inner thigh without covering with . The orientation of both testes was transversely cranio-caudal in the ventral part of the abdominal cavity and was slightly slanted in a medio-lateral (Fig. 1). The average weight of the testes (1.15± 0.10, 1.13± 0.02 gm) left and right respectively showed in Table 1. The epididymis showed as a long convoluted tubule firmly attached to the dorsal border of testis and runs along its entire length cover the cranial pole of testis and project from the Fig. 1. Ventral anatomical views for the reproductive caudal pole of the testis. It consisted of head narrow system of male long eared hedgehog shows in A) The body and tail, the average length of the epididymis was morphology of penis (p) and testis (t). B) Shows the sigmoid flexor (s), free part of penis glans (f), body (b), root (r). C) (38.32± 0.31 mm; 38.09±0.28 mm) left and right Illustrates the position of Intra-abdominal testis (t) and penis respectively, the continuation of the tail of epididymis (p). D) Shows ductus deference (dd) and epididymis (ep), appeared as a muscular straightened tube head of epididymis (h), body (b), tail (t) E) Shows testis (t), (Fig. 1). ductus deference (dd), seminal vesicle (sv), prostate (p), The penis in long eared hedgehog appeared to have urinary bladder (ub). F) Shows bulbourethral gland (bu) and a cylindrical shape consisted of free part, body and rectum (re) crura. The crura of penis were attached to the ischiatic arch by ischiocavernous muscle. The penis when was mid-ventral abdominal wall was opened. Then, the retracted located ventrally to the pelvic symphysis and ischiatic arch was removed to expose the genital organ. abdominal wall under the skin. It was directed caudo- All measurements were obtained instantly after body ventrally then turns cranially to reach the umbilical by dissection for the penis, testes and accessory sex prepuiteal orifice, and was U shaped and slightly slanted glands. Thereafter, each specimen was dissected and to the left side (Fig. 1). It had also a two ribbon of examined to evaluate the organs grossly. retractor muscle extended dorsally along the penis (Fig. Histological procedure 1). The length of the penis was (36.6±2.15mm). The Specimens of the penis, testes and accessory sex body of the penis had a sigmoid flexure. The glans penis glands were sectioned and fixed in neutral buffered of the free part was completely covered with prepuce formalin (NBF) 10% about 48 hours, dehydrated in when retracted penis. The dorsal surface of the glans progressive ethanol cleared in two jars of xylene and penis had a two nail like structures on both side of small then embedded in liquid paraffin and blocked. Slices of urethral process (Fig. 1). 6 μm were stained with (HandE), Masson Trichrom and Grossly, the sex glands were consisted of the periodic acid Schiff reagent (PAS) (Banchroft et al., seminal vesicle, prostate and bulbourethral glands and 1996). Measurements of the tissues were calculated and absent of ampullae of ductus deferens. The biometric

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Table 2. Biometric data shows epithelial thickness for the parts of the reproductive tract in male hedgehog (µm) (n=6) Capsule thickness (µm) tubular diameter (µm) Luminal Diameter (µm) Height epithelium (µm) Testis 47.14±6.99 184.29±15.91 52.86± 14.85 60±7.56 Epidydmis 57.14±3.64 166.43±5.15 98.57±5.15 42.14±2.47 SV 21.67±4.71 346.67±48.19 281.67±58.14 28±2.24 Prostate 136.16±26.76 336.17±32.56 226.67±30.91 61.17±29.26 BU 107.5± 17.97 201.67±21.92 145.83±28.93 23.33±3.73

data were showed in Table 1. Seminal vesicle gland appeared to have a paired (left and right) lobes, heart shaped of white pinkish color lobulated in appearance located dorso-laterally to the urinary bladder and ductus deference. It was detected to be separated at each sides into to two lobes: dorso-medial and ventro-lateral parts (Fig. 1). It was converged caudally toward the neck of bladder as a two duct parallel with the ductus deferens to penetrate the . It had extremely very large size with the average length (30.24±1.76 mm) and width (34.75± 2.03 mm). It was observed extended to reach to the abdominal cavity. The prostate gland was observed to be a paired (left and right) lobes, oval shaped of yellowish in color, the dimensions of gland include length width, and thickness Fig. 2. Photomicrographs illustrate in A) cross sections of were (21.948± 0.49, 29.292± 0.72, 7.18± 0.45mm) the testis shows seminiferous tubules (s), interstitial tissue respectively, and were situated ventro-laterally to the (i), tunica albugina (ta), (tv) and blood urinary bladder and ductus deference (Fig. 1). The vessels (bv). B) Shows basement membrane (b), myoid bulbourethral glands were consisted of two lobes, fleshy, cells (m), Lydig cells (l), spermatogonia (spg), disc-like structure, brown in color, smooth shining (spc), (spd), spermatozoa (spz), surface with no external lobulation in fresh state, sertoli cells (s). C) Shows spermatozoa (s), stereocilia of secretory cell (black arrow). D) The cross section of the situated extra pelvic cavity, at both sides of the rectum pensis shows tunica albugenia (ta), corpus cavernosum under the skin and on the ischiocavernosus muscle (Fig. penis (ccp), corpus spongiosum penis (csp), urethra(u), 1). The gland had a single excretory duct drill the wall of dorsal veins (dv), retractor skeletal muscle (sk), whereas (a) pelvic urethra at the crura of penis. The average weight represents the high magnification of corpus spongiosum was (1.20± 0.07, 1.16±0.05 gm) respectively of left and penis. (A stained with PAS, B and C stained with H&E and right lobes. The duct of these glands continued to medio- scale bar= 100 µm, while D stained with the Masson cranial part and entered to the pelvic urethra Trichrom stain and scale bar=200 µm) dorsolateral. Ductus deferens was found without any enlargement in its terminal part and located under the myoid cells. The interstitial tissue around the tubules ventral surface of the seminal vesicle gland when enter was consisted of loose connective tissue, blood and the Culiculus seminals of the urethra. lymphatic vessels, and interstitial cells with a polyhedral shape and oval nucleus (Fig. 2). Histological examination The epididymis showed its basement membrane Microscopical examination of male reproductive enriched with myoid cells that supporting the system in the long eared hedgehog Hemiechinus auritus pseudostratified columnar epithelium and secretory cells at sexual activity showed that the of of which stereocilia design. These epithelial cells were testis was thick, about (47.14±6.99 µm) in average formed from principal and basal cells, the main cells had (Table 2). It was formed from dense connective tissue stereocilia directed to the lumen of the epididymal duct with smooth muscles fibers and large quantity of with elongated nuclei. While the basal cells had collagen fibers, with fibroblasts, thickening in dorsal part spherical nuclei and also spermatozoa were present in to form which sent septa to divide the the epididymis (Fig. 2). testis into lobules. The tunica albuginea was coated by the visceral layer of the vaginalis tunica, composed of Accessory sex gland connective tissue with fibroblasts interweave with blood Microscopical examination of the vesicular gland vessels. The stratified germinal epithelium was at showed that the secretory units present as tubule-alveoli different levels of development with Sertoli cells (Fig. 2). with a wide lumen filled by a non- homogenous secretory Spermatogonia, primary, secondary spermatocytes, product, the lining mucosa have folded and consisted of spermatids, and spermatozoa were found in the simple columnar epithelium with basally elongated epithelia of seminiferous tubules that was appered to be nuclei and gradually the height of epithelium reduced supported by basement membrane with presence of when the lumen of secretory unit filled with secretions

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DISCUSSION The morphology of male genital system of Hemiechinus aurtus in some aspects is differs from that general pattern described for ; so, many of these certain characteristics are shared by other insectivores (Collins et al, 1982; Woodall,1995; Bedford et al, 1999; Bordignon and Adriana 2012) and many of rodents (Weir,1974; Contreras,and Bustos- Obregón,1980) Some of these features are noted in some types of bat, mole, Hystricomorph Rodents, Spalocopus and Abrocoma. In general, the testes are located in the inguinal canal or abdomen, because there is no true scrotum. In fact, unlike to other insectivores, (Kwiecinski, and Thomas,1999; Krutzsch et al,2002; Nogueira et al, 2004) and carnivores (Halıgür et al, 2019), which have a testes in well-developed scrotum. Fig. 3. Photomicrographs illustrate the histological The presence of scrotal testis may be cited as features, structures of the accessory sex glands in male long eared which coincide to the primate pattern (Luckett, 1980; hedgehog. A) Cross section of the bulbourethral gland shows stroma (st) of the gland and simple columnar (s) of Praxedes, 2018), therefore the insectivores consider as the secretory tubule-alveolar unit (se). B) Shows the a low primate than . The orientation of the secretory units of prostate gland lined with simple low hedgehogs testes in this study transversely cranio- columnar to cuboidal and sometime stratified epithelium caudal in the ventral part of the abdominal cavity and and folded of lining mucosa (black arrows). C) Shows the was slightly slanted in a medio-lateral is similar to secretory units of vesicular gland observed filled by a non- Neotropical Rodent Agouti (Mollineau, 2006). Also the homogenous secretory product and folded of lining mucosa style and coloration of the testes are coincide with the lined with the simple columnar epithelium (black arrows). study of (Mollineau, 2006) in agouti, (Beguelini et al, (A, B, C stained with H&E and scale bar= 100 µm) 2013) in bats. As observed from this study, the epididymis hedgehog had significant similarity to that of (Fig. 3). The epithelium of the follicular secretory units of other mammals consists from three parts head, body prostate gland appeared as a simple low columnar to and tail. The penis of the long eared hedgehog cuboidal and sometime showed as a stratified examined in the current study had the general pattern epithelium. The secretory follicles showed different size observed in mammals, which easily determine three according to the activity of secretion also, the mucosa regions, glans, body and crura, and directed cranially, had a folding shape (Fig. 3). Bundles of skeletal muscles this result disagree with the result of (Mollineau, 2006) intermingle with dense irregular connective tissue to who mention that the penis of agouti was posteriorly from a thin capsule that surrounded the bulbourethral directed, and in agree with (Woodall et al, 1995) in gland, trabeculae of loose connective tissue derived elephant . The glans penis was well developed from the capsule to divided the parenchyma of the gland and had a two nail like structures dorsally, these into lobules that contained secretory units, the stroma of structures may be designed for increased stimulation of the gland is consist of dens irregular connective tissue female vagina and also be found in agouti (Mollineau, and had a smooth muscle fibers. The simple columnar 2006), and some species of bat (Comelis et al, 2018) epithelium was lined with the secretory tubule-alveolar also, in other mammalian species have stimulated units. The epithelial cells contain oval nuclei (Fig. 3). The ovulation. The presence of urethral process, sigmoid penis showed paired corpus cavernosum, each of it was flexures also the two ribbon of retractor muscle make the surrounded by dense connective tissue that called hedgehog penis similar to that of ruminants. Therefore tunica albugina which sent septum that separated the penis of long eared hedgehog is considered as between two corpus cavernosum. The tunica albugina intermediate type penis. The anatomy of the genital formed from bundle of collagen fibers and smooth glands in the male hedgehog is different from that in muscles fibers. The trabeculae between the other Insectivora. For instance, there was no ampulla cavernousum which derived from tunica albugenia ductus deference in this . Unlike other Insectivora, formed the spaces lined with endothelium and it presence three types of glands only, seminal vesicle, surrounded by dense irregular connective tissue to form bulbourethral glands, and coagulating glands. It has also the erectile tissue. The corpus spongiosum penis, been recorded that ampullae glands are not developed entirely surrounded the penile urethra. The penile in the rat (Gottreich et al, 2001), greater cane urethra was lined by transitional epithelium, which was rat (Adebayo, and Akinloye, 2009), agoti (Mollineau, transformed into stratified squamous epithelium toward 2006). Furthermore, it has been indicated that vesicular the tip of the glans penis (Fig. 2).

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EurAsian Journal of BioSciences 14: 6657-6663 (2020) Jabbar et al. glands there are absent in the agoti (Mollineau, 2006) and Akinloye, 2009), who mentions that the seminal and blind mole rat (Gottreich et al, 2001),while in resent vesicle of great cane rate was branching tubule-alveolar study the vesicular gland was largest of the accessory secretory unit. The luminal diameter, height of mucosal sex glands separated at each sides into to two lobes folds and height of epithelium were according to the dorso-medial and ventro-lateral parts and extended to sexual activity of the male. But the seminal vesicle ducts the abdominal cavity. The variety of combinations of join the urethra separately from the ductus deference. accessory sex glands may be due to environmental This result disagree with the (Collins et al, 1982), who temperature, hibernate period, type of diet, sexing report that there was an in the shrew. behavior, or even genetic variation between species. The, scrotal testis, pendulous penis, paired seminal Microscopic examination of the testes appeared to vesicles, and an ejaculatory duct may be cited as have all cellular stages of and sertoli features which coincide to the primate pattern and differ cells. The interstitial tissue filled the space between the from the arrangement of most insectivores. However, tubules, where different diameter blood vessels and the absence of the ampulla ejaculatory duct and scrotum capillaries were showed. The different gametogenic in the hedgehog consider as characteristic features of cells showed in the seminiferous tubules were coincided insectivores and different from those found in higher to results recorded by (Collins et al, 1982; Praxedes, . According to the activity of secretion the 2018) and other insectivores. Observation all the types epithelium of secretory unit was varied from of germ cell in the seminiferous tubules, spermatozoa in pesudostratified to the low cuboidal also the epithelial the tail of epididymis and a large number of leydig cells folding. in interstitium indicated that the time of our sampling at Previous study reported a pseudostratified columnar the time of spermatogenesis. These results are in epithelial that lining the prostate in the agouti is agreement with what the researchers reported that the (Praxedes, 2018). However, it is simple columnar in the height testicular weight occurs when the seminiferous guinea pig (Cordeiro, 2004), also the (Akbari, and tubule diameter due to high spermatgenic activity and Davoud, 2017) report that the prostate gland of Persian plasma testosterone level are maximal. Several studies squirrel is lining with simple cuboidal. The prostate (Banks, 1993;30) indicated that, from interior to exterior, glandular epithelia range from cuboidal to columnar in the microscopical structure of the penis in laboratory and mammalian (Samuelson, 2007). The bulbourethral domestic animals is a composed from; lamina interna of gland in the present study was tubule-alveolar type and preputium, epidermis of penis, tunica albuginea (fibrous lined by simple columnar epithelium, this results were type penis), cavernosum penis, spongiosum penis, and similar to earlier authors (Danmaigoro, 2014; Banks, epithelium of urethra. All these microscopical structures 1993, Samuelson, 2007), as they described that the were showed in the long eared hedgehog. According to bulbourethral glands are compound tubular in boars, (Banks, 1993), the urethra when entering glans penis cats, bucks; tubuloalveolar gland in bulls, rams, stallions will be wide, and gradually the lining epithelium of and in human and absent in dogs. urethra changed from domestic into stratified squamous epithelium. This result was found to be fully the same for CONCLUSION hedgehog. The thick tunica albuginea in this study is The genital system of the male long eared hedgehog similar to (Konig, 2009) and well developed basement had both variations and similarity to the other membrane is considered as deference mechanism to insectivores species. The penis of hedgehog was fibrous sperm from the body temperature in abdominal testis type correspond to that of ruminants in presence of animals. (Banks, 1993; Samuelson, 2007) recorded that urethral process, sigmoid flexures also the presence of the penis has two types, well developed tunica two ribbon of retractor muscle and directed cranially, but albuginea in (fibrous penis type) and thin tunica similar to that of insectivores of having glans with two albuginea and erectile tissue had a lot of surface area in nail like structure. The anatomy of the hedgehog male the (vascular penis type), so the same authors explain accessory genital glands was various from that in other that according to this classification, the pigs and Insectivora being no ampulla ductus deference in this ruminants tunica albuginea is well developed, consisting animal, therefore the accessory sex gland include of dense connective tissue and forming a fibrous type largest seminal vesicle, prostate, and bulbourethral. penis. In the transverse sections, it was illustrated that According to histological observations, we illustrate that the penis covered by a thick sheath of connective tissue the male genital system of long eared hedgehog, follows called the tunica albuginea. Therefore, in the the normal mammalian pattern, and were at sexual the diameter of the penis not increased but the length of activity season. penis will increase. But, most of the increase in length of penile is due to the straightening of the sigmoid flexure. ACKNOWLEDGEMENTS The histological structures of the accessory sex glands: seminal vesicle, prostate and bulbourethral The authors strongly acknowledge the staff of glands were found in agree with the study of (Adebayo, Department of Anatomy College of the Veterinary

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Medicine / University of Diyala to support this research project.

REFERENCES Adebayo A, Oke B O, and Akinloye A K (2009). The gross morphometry and histology of the male accessory sex glands in the greater cane rat (Thryonomys swinderianus, Temminck). Journal of Veterinary Anatomy, 2(2), pp.41-51. Akbari G and Kianifard D. (2017). Anatomy, histology and histochemistry of accessory sex glands in male Persian squirrel (Sciurus anomalus). Italian Journal of Anatomy and Embryology, pp.17-26. Banchroft J D, Stevans A, and Turnes D R (1996). Theory and Practice of Histological Techniques 4th ed., livingstone. Edinburgh, London, Melbourne, New York, Tokyo. Banks W J (1993). Applied veterinary histology. Mosby-Year Book, Inc. Bedford J M, Mock O B, Nagdas S K, Winfrey V P, and Olson G E (1999). Reproductive features of the (Scalopus aquaticus) and star-nose mole (Condylura cristata). Reproduction, 117(2), pp.345-353. Beguelini M R, Puga C C, Martins F F, Betoli A H, Taboga S R, and Morielle‐Versute E (2013). Morphological variation of primary reproductive structures in males of five families of neotropical bats. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology, 296(1), pp.156-167. Beguelini M R, Cíntia CI P, Fabiane F M, AndrÉ HS B, Sebastião R T, and Eliana M V (2013) Morphological variation of primary reproductive structures in males of five families of neotropical bats. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology 296, no. 1 (2013): 156-167. Çolak E, Yiğit N, Sözen M And Özkurt Ş, (1998) A Study on the Long-eared hedgehog, Hemiechinus auritus (Gmelin, 1770)(Mammalia: Insectivora) in Turkey. Turkish Journal of Zoology, 22(2), pp.131-136. Collins P M, Tsang W N, and Lofts B (1982). Anatomy and function of the reproductive tract in the captive male tree shrew (Tupaia belangeri). Biology of Reproduction, 26(1), pp.169-182 Comelis M T, Bueno L M, Góes R M, Taboga S R, and Morielle-Versute E (2018). Morphological and histological characters of penile organization in eleven species of molossid bats. Zoology, 127, pp.70-83. Contreras L. and Bustos-Obregón E. (1980). Anatomy of reproductive tract in Octodon degus Molina: A Nonscrotal rodent. Archives of Andrology, 4(2), pp.115-124. Corbet G B (1988). The family Erinaceidae: a synthesis of its taxonomy, phylogeny, ecology and zoogeography. review, 18(3), pp.117-172. Cordeiro R S, Scarano W R, Góes R M and Taboga S R (2004). Tissue alterations in the Guinea pig lateral prostate following antiandrogen flutamide therapy. Biocell, pp.21-30. Danmaigoro A, Onu J E, Sonfada M L, Umaru M A, Hena S A, and Mahmuda A, (2014). Gross and morphometric anatomy of the male reproductive system of bats (Eidolon helvum). Veterinary medicine international, 2014. Fard E A and Ghassemi F (2017). Histological and morophometrical study of male reproductive tract in Rousettus aegyptiacus (Mammalia: Megachiroptera) in Iran. Journal of Entomology and Zoology Studies, 5(1), pp.229-234. Gottreich A, Hammel I, Yogev L, Bartoov B. and Terkel J (2001). Structure and function of accessory sex glands in the male blind mole rat (Spalax ehrenbergi). Journal of mammalogy, 82(1), pp.201-208. Halıgür A. and Özkadif S (2019) Male Genital Organs in the Red Fox (Vulpes vulpes); Macroanatomic and Three- dimentional Reconstruction Aspect. Mehmet Akif Ersoy Üniversitesi Sağlık Bilimleri Enstitüsü Dergisi, 7(2), pp.89-98. Hijikata T, Saito H and Yohro T (1986). Anatomy and histology of the musk shrew ( murinus) prostate. The Prostate, 8(3), pp.277-291. Hutterer R (2005) Order Erinaceomorpha. Mammal species of the world: a taxonomic and geographic reference (DE Wilson and DM Reeder, eds.). 3rd ed. Johns Hopkins University Press, Baltimore, Maryland: 212-219. Konig H E, Liebich H G, and Cerveny C (2009). Veterinary Anatomy of Domestic mammals Text Book and Color Atlas,(pp. 489-518). Krutzsch P H, Fleming T H, and Crichton E G (2002). Reproductive biology of male Mexican free-tailed bats (Tadarida brasiliensis mexicana). Journal of Mammalogy, 83(2), pp.489-500. Kwiecinski G G, and Griffiths T A (1999). Rousettus egyptiacus. Mammalian Species, (611), pp.1-9.

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Luckett W P (1980). The suggested evolutionary relationships and classification of tree shrews. In Comparative biology and evolutionary relationships of tree shrews (pp. 3-31). Springer, Boston, MA. Mollineau W, Adogwa A, Jasper N, Young K and Garcia G, (2006). The gross anatomy of the male reproductive system of a neotropical rodent: the agouti (Dasyprota leporina). Anatomia, histologia, embryologia, 35(1), pp.47- 52. Nogueira J C, Castro A CS, Câmara E V C and Câmara B G O (2004) Morphology of the male genital system of Chironectes minimus and comparison to other didelphid marsupials. Journal of Mammalogy, 85(5), pp.834-841. Praxedes E C G, Peixoto G C X, da Silva A M, and Silva A R (2018) Reproduction in agouti (Dasyprocta spp.): A review of reproductive physiology for developing assisted reproductive techniques. Animal Reproduction (AR), 15(4), pp.1181-1192. Reiter C and Gould G C (1998) Thirteen Ways of Looking at a Hedgehog. Natural history, 107(6), pp.52-56. Roberts T J and Bernhard (principe d’Olanda.), (1977) The mammals of Pakistan. Samuelson D A (2007). Textbook of veterinary histology (No. V200 SAMt). Weir B J (1974) Reproductive characteristics of hystricomorph rodents. Symp Zool Soc Lond 34: 265–301. The Biology of Hystricomorph Rodents. Academic Press Inc, London. Woodall PF (1995) The male reproductive system and the phylogeny of elephant‐shrews (Macroscelidea). Mammal Review, 25(1‐2), pp.87-93.

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