Anatomical aspects of the male reproductive system in the bonnet ...

Anat Sci Int (2009) 84:53–60 DOI 10.1007/s12565-008-0007-9

ORIGINAL ARTICLE

Anatomical aspects of the male reproductive system in the bonnet monkey (Macaca radiata) S. Prakash Æ S. Suresh Æ E. Prithiviraj

Received: 26 June 2008 / Accepted: 27 August 2008 / Published online: 17 February 2009 Ó Japanese Association of Anatomists 2009

Abstract The normal anatomy of the male reproductive system in Macaca radiata is presented here. The external genitalia consist of a triangular button-shaped glans penis. The corpus cavernosum, and spongiosum form the vascular component of the penis and the baculum or os penis forms the non-vascular erectile component. The baculum is one of the longest in the genus macaques. The scrotal sac is non-pigmented, slightly pendulous, with scattered hairs, faintly corrugated, and does not reach the ischial callosities in the sitting posture. The testicles are ovoid in shape without appendix. Right and left testicular arteries originate at the level of the inter-vertebral disc between T12–L1 and L2–L3, respectively. Seminiferous tubules present mixed stages of spermatogenesis, i.e. single/multistage. The epididymis is crescent shaped, attached to the posterolateral border of the testis without an appendix. Light microscopic observation revealed a characteristic high columnar epithelium with stereocilia. Clear cells or light cells are seen in the caudal region. The ductus deferens display a lumen lined by pseudo-stratified columnar epithelium separated by concentric layers of smooth muscle cells covered by serosa. The seminal vesicles are pyramidal in shape, prominently projecting above the urinary bladder, and are the largest of the accessory glands, typical of polyandrous primate genera. The prostate is conical in shape. Its base is in contact with the trigone of the bladder. Its posterior surface shows a transverse cleft separating an upper quarter, the cranial lobe, from the lower three-

quarters of the gland. Compared with other macaques there are many distinguishing features in M. radiata. Excellent adaptability and spermatogenic efficiency in the laboratory environment makes this animal a good primate model for andrological research. Keywords Macaca radiata Testis Epididymis Accessory sex organs Morphology

Introduction In the last few decades Macaca radiata has been the preferred non-human primate model in endocrinology, screening of contraceptive vaccines, reproductive biology, and neural-transplantation studies in India. Although extensively used for various research, surprisingly, very little published literature is available about the normal biology, behaviour, and diseases of M. radiata (Ramakrishnan and Mohan 1962; Srikantia and Gopalan 1963; Ovadia et al. 1971; Flechon et al. 1976; Jensen et al. 1980; Jayaraman et al. 1980; Kenyon et al. 1992; Rao et al. 1997; Taylor et al. 1998; Sankar et al. 2000; Prakash et al. 2001, 2008). In this study the normal anatomical features of the male reproductive organs (testis, epididymis, ductus deferens, prostate, seminal vesicle, and penis) of bonnet monkeys were analysed.

Materials and methods S. Prakash (&) S. Suresh E. Prithiviraj Department of Anatomy, Dr. Arcot Lakshmanasamy Mudaliar Postgraduate Institute of Basic Medical Sciences, University of Madras, Taramani Campus, Chennai 600 113, India e-mail: [email protected]

This study was performed on eight adult male monkeys. The animals required for this study were procured from the Wild Life Park at Guindy in Chennai after obtaining permission from the Conservator of Forests, Tamil Nadu.

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Healthy Adult male monkeys of body weight ranging from 6 to 8 kg were selected for the study. Fertility of the animals was confirmed by semen analysis during a quarantine period. Quarantine and animal maintenance were carried out according to the guidelines formulated by international (Canadian Council) and local bodies (Laboratory Animals, India). The ethical committee of Dr A.L.M.PGIBMS, University of Madras, approved the protocol of the work. Details of animal maintenance have been described elsewhere (Prakash et al. 2001). Tissue harvesting Animals were sacrificed by intraperitoneal administration of an overdose of the anaesthetic thiopentone sodium (Pentothal Abbott Laboratories, India). Immediately after respiration ceased, the animals were fixed by trans-cardial perfusion with formal saline, after flushing the blood with normal saline, and the required tissues were stored in Bouin’s fixative till further processing. Tissues were processed by the paraffin technique and sections were taken at 7 lm thickness. Sections stained with Delafield haematoxylin and counter stained with eosin were used for histological and histmorphometric observations, as described elsewhere (Prakash et al. 2008) and values are given in relative terms.

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6 ± 0.81 cm and the radix or root was about 11 ± 0.42 cm. Circumferential diameter was 4 ± 0.78 cm. During erection the body or free part of the penis can increase up to 10 ± 1.4 cm. The prepuce is always retracted in a position exposing the glans penis; during erection the prepuce exposes the major part of the body of the penis. The glans penis is triangular or button shaped. The scrotal sac is slightly pendulous with the penis projecting from the midline; anteriorly the lowermost part of the sac does not reach the ischial callosities. The skin of the scrotal sac is non-pigmented and bears scattered hairs and faint corrugations, and the testis fills the sac when the animal is in the sitting posture, giving almost a smooth appearance to the scrotum (Fig. 1a). When the animal stands upright on its hind limbs the testes are raised and pulled towards the superficial inguinal ring near abdominal wall and the scrotum appears shrivelled and emptied. Deep in the scrotal skin was the poorly developed tunica dartos and the connective tissue extending into the scrotal septum. No distinct median raphe is seen either in the scrotal sac or in the ventral side of the penis. Regarding the erectile component of the penis, the hydrostatic elements corpus cavernosum and the corpus spongiosum contribute the vascular component. The baculum or os penis contributes the non-vascular erectile structure of the penis, and is approximately 2 ± 0.55 cm in length and 3 ± 0.92 mm in diameter (Fig. 1b).

Analysis of spermatogenic stages Testis Two different types of tubular arrangement are seen in terms of spermatogenic stages, i.e. single stage (one spermatogenic stage per tubular cross-section) or/and multistage (more than one spermatogenic stage per tubular cross-section), on the basis of the spermatogenic cycle (Clermont and Antar 1973). One-hundred seminiferous tubules per testis were analyzed and evaluated. Only tubular cross-sections with circular profile were examined. This was expressed in terms of the relative stage frequency as follows: RSFstage = 100/N 9 nstage (%), where, RSFstage is relative stage frequency, N is the sum of all stages divided by 100 tubular cross-sections, and nstage is the number of the specific stage per 100 tubules (Wistuba et al. 2003). Data were analysed using Microsoft Excel for Windows and values are expressed in % or as ±standard deviation of the mean.

Results

The testicles are ovoid in shape situated at the same level when they are inside the scrotal sac. The testicles are covered by the tunica vaginalis. Each testis is compressed from side to side and its upper pole tilted postero-laterally and the lower pole tilted antero-medially, average length, breadth, and width are 3.8 ± 0.22, 2.5 ± 0.18, and 2.6 ± 0.12 cm, respectively. Anterior aspect is convex; posterior aspect is straight. Extending along its superior and postero-lateral border is the epididymis. Appendix of testis is absent. Right and left testicular arteries originate from the abdominal aorta, at the level of inter-vertebral disc between T12–L1 and L2–L3, respectively (Fig. 1c). Microscopic examination of the stained slides revealed a normal testicular pattern as described earlier by Flechon et al. (1976). In addition to existing knowledge, in this study the percentage of single/multistage spermatogenic tubules and other morphometric data are presented (Table 1, Fig. 2a, b).

External genitalia

Epididymis

In adult animals the average total length of penis was about 17 ± 1.2 cm. The corpus or body of the penis was about

This was crescent shaped, attached to the postero-lateral border of the testis, approximately 4.2 ± 0.31 cm long.

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Male reproductive system in bonnet monkey

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Fig. 1 a External genitalia of bonnet monkey showing scrotal content and penis. b Transverse section of the penis. Note the ossified structure baculum or os penis (arrow), erectile tissue (X) and k-shaped urethral orifice surrounded by urethral musculature (arrowhead). c Morphology of testis (T), epididymis (E), and ductus deferens (D). d Morphology of seminal vesicle (SM), prostate (P) and urinary bladder (UB). Note the demarcation seen between the cranial and caudal lobes of the prostate (arrow)

Table 1 Morphometry of testis Studied characteristics of the testis

Values ± SD

Testicular volume (cm3)

11.3 ± 2.56

Diameter of the seminiferous tubule (lm)

330 ± 4.29

Seminiferous epithelial height (lm)

75 ± 0.51

Relative volume of seminiferous tubules (mm3/mm3) 0.967 ± 4.21 Seminiferous epithelial volume (mm3/mm3) Number of Leydig cells (per mm3)

0.566 ± 6.95

Light microscopic examination of the epididymis revealed the normal histological pattern as described by Flechon et al. (1976) with characteristic stereociliated pseudo-stratified columnar epithelium cells averaging 70 ± 2 lm in height attached to the basement membrane, which is surrounded by smooth muscle fibres. The clear cells or light cells are seen predominantly in the caudal region (Fig. 2c, d).

142 ± 4

Ductus deferens

Spermatogenic stage Multiple (%)

37 ± 3.68

Single (%)

62 ± 6.17

The upper half of the epididymis has a mesentery. It is the continuation of the mesentery of the spermatic cord. The epididymis has a superior enlarged head or initial segment followed by body or middle segment and tail or terminal segment. The head is attached to the upper pole of the testis by the ductus efferent and the tail continues as the ductus deferens, which passes upwards along its medial side. Appendix of epididymis is absent (Fig. 1c). Morphometry data are presented in Table 2.

This runs along with testicular artery and veins in the spermatic cord and, after crossing the ureter, converges towards the median line of the upper part of the prostate. Near the pelvic part close to the prostate the duct is slightly expanded, but no clear ampulla is observed. However, zigzag bending of the ductus deferens are seen in this region. The duct passes antero-medially between the posterior surface of the bladder and upper pole of the seminal vesicle; the total length is approximately 11 ± 1.3 cm. The duct then narrows and joins the duct of the seminal vesicle to form an ejaculatory duct. The prostatic ends of the ductus deferens are obviously thicker than the testicular end in these animals. At both ends the ductus deferens

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Fig. 2 a, b Photomicrographs of testis showing normal stages of spermatogenesis. Sp, spermatogonium; Psp, primary spermatocytes; ES, early spermatids; LS, late spermatids. Scale bar represents 100 and 15 lm for a and b, respectively. c Photomicrograph of caput region of epididymal tubules lined by pseudo-stratified epithelium with stereocilia. Note the principal (white arrowhead), apical (black arrowheads), basal (white arrow), and clear cells (C). Scale bar represent 80 lm. d Photomicrograph of caudal region of epididymal tubules showing similar epithelial lining but with lengthier epithelium than caput. Note the predominant stellate lumen (stars) of the ductal sections in the region. Scale bar represent 80 lm. e Photomicrograph of seminal vesicle showing glandular epithelium. Note secretory products stored in one of the vesicles (star). Scale bar represent 80 lm. f Photomicrograph of prostate showing tubo-alveolar gland with secretory epithelial lining, surrounded by connective tissue stroma. Scale bar represent 80 lm

Table 2 Morphometry of the epididymis

Studied characteristics of the epididymis Epididymal volume (cm3) Diameter of the epididymal tubule (lm) Epididymal epithelial height (lm) Epididymal tubular volume (mm3/mm3)

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Caput

Corpus

Cauda

370.64 ± 3.55

330.69 ± 7.38

310.41 ± 6.5

71.0 ± 0.71

58.34 ± 2.84

52.80 ± 1.8

0.752 ± 0.35

0.624 ± 0.40

0.672 ± 0.50

4.3 ± 0.31


display a lumen lined by pseudo-stratified columnar epithelium separated by concentric layers of smooth muscle cells covered by serosa. The muscular layer consists of inner and outer circular layers and an intermediate longitudinal layer; the lumen to wall ratio gradually increases starting from the testicular end towards the prostatic end. The average height of epithelial cells is approximately 30 lm with stereocilia protruding into the lumen; the nuclei of these cells are located in the basal half. The lumen showed a number of longitudinal folds of epithelia. Seminal vesicles These are lobulated masses, more or less pyramidal in shape, prominently projecting above the urinary bladder. They are the largest of the accessory glands. They are coiled tubes with an irregular diverticulum, which is connected by fibrous tissue (Fig. 1d). The seminal vesicle is a storage gland lined with pseudostratified columnar epithelium. In the cephalic region or in the lateral region, the epithelium shows numerous folds of invagination. In the central region or the medial portion, folds of the epithelia invagination are reduced. Epithelial cells are directed towards the lumen from the lamina; the nuclei are placed at different heights in the epithelium. They are large and ovoid or spherical in shape (Fig. 2e). Prostate This is conical in shape, with the base in contact with the trigone of the bladder. The gland is situated posterior to the proximal part of the urethra, which is close to the prostate. Its posterior surface showed a transverse cleft separating an upper quarter, the cranial lobe, from the lower threequarters, or caudal portion, of the gland. The rest of the prostate is a single mass without any distinct lateral lobes (Fig. 1d). The ejaculatory ducts perforate the cranial lobe and open into the prostatic urethra, which is 1 cm long and corresponding in extent to the prostate. The epithelium forms multiple compound tubo-alveolar glands. Glands appear as irregularly circular, oval, and curving alveoli or sacculus lined with columnar epithelium, which have basally located nuclei. The epithelium has an undulating contour and frequently projects as folds into the lumen. The interstitial tissue fills the space between the epithelial elements and forms sheets or septa that separate and invest the alveoli. The interstitial tissue is composed of smooth muscle and fibrous tissue. Each acinus showed numerous epithelial folds consisting of columnar cells (Fig. 2f). The prostatic urethra is lined by transitional epithelium. The bulbo-urethral glands are poorly developed and situated near bulbar region of the urethra, draining their secretion in to the urethra.

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Discussion Macaca mulatta and M. fascicularis have been used extensively for research. The general anatomy, physiology, and behaviour are well recorded for these non-human primates. The species M. radiata is distributed in the Indian peninsula and used for various experimental studies. Surprisingly, very few reports have been published on the normal anatomy of this species, especially the male monkey. Rao et al. (1998) described sexual maturity, menstrual cyclicity, general behaviour, endocrine profile, reproductive physiology, gestation, parturition, and postpartum amenorrhoea in the female, and a few characteristics of the male monkey, for example sexual maturity, hormone profile, and seasonal variation in sperm count. Although this study was a comprehensive report of bonnet monkey biology, there was little anatomical description of male. Macaca radiata is a continuous breeding animal with a peak during the months of October to December (Rao et al. 1997; Bansode et al. 2003). During these months, the monsoon and cold seasons are the usual climate in this part of the world. Obviously the environmental temperature in that season should be favourable for spermatogenesis, after a long and hot summer season. Thermoregulatory mechanisms, for example pendulous scrotum, pigmented skin, and corrugation, are limited in this animal. Probably this could be among the reasons for the reduction in the reproductive capability in other months when the environmental temperature varies from the optimum temperature for spermatogenesis. It is worth mentioning here the position of the testis in this animal. When the animal stands upright on its hind limbs the testes are raised and pulled along with the spermatic cord towards the superficial inguinal ring near abdominal wall, because of the shortness of the cord and their permitted mobility in the inguinal canal and scrotum. Hence, when performing experiments involving surgical procedures in this region, one should be careful of cryptorchism as a major post operative complication. During any non-invasive procedures of the scrotal contents, for example ultrasonography, positioning of the hind limb is very important to avoid misinterpretation of lesion sites (Prakash et al. 2002). The testes are normally present in the scrotal sac when the animal is in its sitting posture. In the cold season the body warmth of the other animals may protect the testis, as these monkeys have the habit of remaining together when present in groups (Jensen et al. 1980). Annual variation in testicular volume of adult M. radiata under laboratory conditions is similar to the description by Glick (1979) and similar to the pattern of variation reported for the other species M. fuscata (Matsubayashi and Enomoto 1983) and M. mulatta (Wickings and Nieschlag 1980).

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The normal sitting position itself may protect the testicles from direct exposure to the environment. These observations suggest that the testis in this animal is vulnerable to change in its natural environmental temperature, however, in terms of seasonal variation of spermatogenesis in M. radiata it was less affected than M. mulatta (Gupta et al. 2000), and these above mentioned anatomical and behavioural adaptations could be playing a major role in this outcome. This was evident from the histology of the testis from new entry from the wild to the colony during the non-breeding season (n = 2). Under a controlled environment, success rate of breeding was increased, indicating its ability to breed continuously throughout the year (Rao et al. 1997). In the wild, breeding seasons are successful every year without immediate threat of endanger; according to the IUCN red alert (2004) report of endangered species, nearly 10,000 adult male monkeys are distributed in southern India. The helmet-shaped glans penis is virtually identical in M. fuscata, M. mulatta, M. cyclopis, and M. fascicularis, and extends dorsally and ventrally along the shaft of the penis (Fooden 1971). No such extensions are seen in M. radiata. Similar to all other primates (with the exception of human, brachyteles, and langothrix) the penis of this monkey contains a baculum (os penis). This is assumed to represent atavism, or the appearance of a characteristic found in remote ancestors but not in nearer ancestors (Hoeg 1986). The presence of the baculum will be helpful for penis erection, stiffness, and vaginal friction. The baculum in M. fuscata, M. mulatta, and M. fascicularis is of similar form; these animals constitute a closely interrelated group based on penile characteristics. But the baculum in M. fascicularis is smaller than in M. fuscata and M. mulatta (Fooden, 1971). Surprisingly, the baculum in M. radiata is longer than in M. fuscata and M. mulatta, which may play a major role in M. radiata copulation. Preliminary M. radiata copulatory behaviour observed in captivity was similar to that described for stumptail macaques (M. arctoides) (Brereton, 1994). In addition to M. radiata testicular and epididymal histological observations reported earlier (Flechon et al. 1976), the histomorphometric results revealed a very much lower proportion of interstitial tissue in adult monkey testis. Similar to other macaques, in M. radiata the membrane separating the seminiferous epithelium from the interstitial space was mainly composed of two layer of myoid cells and is prominent (Prakash et al. 2008).The number of layers is less than that reported in man (two to six layers) (Hermo et al. 1977). Spermatogenic stages in 17 primate species, comprising Strepsirrhini (Prosimians: Lemuriformes, Lorisiformes), Platyrrhini (New World primates: M. fascicularis, M. thibetana (Tibetan macaque), M. nigra (celebes black

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macaque), Catarrhini (Old World primates), and Hominoidea (great apes and humans), were analyzed comparatively by Wistuba et al. (2003), who reported single-stage (one spermatogenic stage per tubular crosssection) or/and multistage (more than one spermatogenic stage per tubular cross-section). In M. radiata the spermatogenic stage was mixed with a frequency of 38% multistage. It has been proposed that the single-stage versus multistage arrangement was related to spermatogenic efficiency and that the multistage arrangement was typical of hominids (Smithwick et al. 1996) and predominant single-stage tubular organization represents the ancestral state (Wistuba et al. 2003). The highest degree of multistage complexity was found in Hominoidea (except orangutan). However, no direct relationship between single-stage/multistage tubular topography and phylogeny could be established across primates, and spermatogenic efficiency was similar in primates both in single and multistage (Weinbauer et al. 2001; Wistuba et al. 2003). The general features of M. radiata epididymis resemble those of all other cercopithecidae. Clear cells or light cells in the epididymides have been described in rat (Hamilton 1975), hamster (Nicander and Glover 1973), and African giant rat (Oke et al. 1988) and are also seen in M. radiata. However, the absence of clear cells has been reported for rhesus monkey (Ramos and Dym 1977), guinea pig (Hoffer and Greenberg 1978), bull (Goyal 1985), goat (Goyal and Williams 1991), and dog (Schimming et al. 1997). Clear cells are regarded as an important component of the mammalian epididymis, because of its presence in the rat epididymis, which is regarded as the prototype of epididymal structure in general. The prostatic end of the ductus deferens of M. radiata forms a moderate dilation with zigzag bending before opening into the ejaculatory duct, unlike the well-formed ampullae in several mammals and which may serve as a sperm reservoir (Cooper and Hamilton 1977; Murakami et al. 1986), including in humans (Nistal et al. 1992). Such ampullae are absent in M. radiata. However, this zigzag bending of the ductus deferens at the prostatic end may reduce the speed of sperm flow in ductus deferens during ejaculations, rather than increase sperm storage. This delay could facilitate secretion by accessory organs and appropriate mixing with sperm, forming a suitable semen mixture (coagulum). The seminal vesicles in M. radiata are well developed and one of the largest in the macaque genera. The seminal vesicles vary greatly in size among primates, being vestigial or rudimentary in some primates (Petter-Kousseaux 1964). The variation in size of the seminal vesicles is related to the mating system; relative testis sizes and copulatory frequencies showed positive correlation in primates (Dixon 1998). With polyandrous mating behaviour


in M. radiata, large seminal vesicles may produce sufficient or major fluid for transport of spermatozoa and formation of a hard copulatory plug. Consequently, the rudimentary Cowper’s gland in M. radiata is compensated. Similarly, compared with the seminal vesicles, the prostate is smaller and less prominent in M. radiata. General morphological description of the prostate was similar to that of M. mulatta (Lewis et al. 1981). Interestingly, biochemical constituents of semen lack seasonal variation in M. radiata (Jayaraman et al. 1980) and thus maintain breeding capability throughout the year. However, the high degree of variation seen in the sperm concentration in this monkey, ranging from 116 to 799 million per ejaculate (Rao et al. 1998), might be a condition seen in captivity and not because of seasonal variation. As far as the authors are aware, normal comprehensive anatomical detail of M. radiata is lacking. This study is an attempt to summarize anatomical features of the male reproductive system. Apart from general adaptive morphological variations of the scrotum, penis, sparse pubic hairs, median raphe, behaviour, accessory glands, etc., seen in M. radiata, adaptability, for example an increase in sperm production in a controlled laboratory environment even in the non-breeding season and good spermatogenic efficiency makes M. radiata as a good primate model for andrological research. Acknowledgments We are extremely grateful for constant support and guidance from Dr V. Sankar, Department of Anatomy, University of Madras, during this study.

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