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From Pubertal Chimpanzees by Masturbation J Cellular and biochemical characteristics of semen obtained from pubertal chimpanzees by masturbation J. Marson, S. Meuris, F. Moysan, D. Gervais, R. W. Cooper and P. Jouannet Centre International de Recherches Médicales, BP 769, Franceville, République Gabonaise, and *Laboratoire d'histologie-embryologie, centre hospitalier, 94270, Le Kremlin Bicêtre, France Summary. Semen characteristics were studied in 6 wild-born chimpanzees with dental ages ranging approximately from 6 to 12 years. The animals formed 2 groups, early pubertal (EP, N = 3, 6\p=n-\9years) and late pubertal (LP, N = 3, 11\p=n-\12years). Mean body weight, testicular volume and serum androgen concentration were significantly lower in Group EP (32\m=.\2\m=+-\1 \m=.\6kg, 34\m=.\0\m=+-\7\m=.\7cm3, 2\m=.\1\m=+-\ng/ml) than in Group LP (55\m=.\7\m=+-\5\m=.\7kg, P < 0\m=.\01;100\m=.\5\m=+-\11\m=.\9cm3, P < 0\m=.\01;3\m=.\6\m=+-\0\m=.\7ng/ml, P < 0\m=.\05). Ejaculates were obtained by masturbation in all subjects. The mean ejaculate volume was lower in Group EP (0\m=.\56\m=+-\0\m=.\20ml) than in Group LP (3\m=.\77\m=+-\0\m=.\73ml, P < 0\m=.\01). In Group EP, 2 animals were azoospermic while the third produced semen with means of 57\m=.\1 \m=x\106 spermatozoa per ml, 20% motility and 40% vitality. These values were low when compared with the mean values of Group LP (376 \m=x\106 spermatozoa per ml, 67% motility and 78% vitality). Mean total sperm count was correlated with testicular volume (r = 0\m=.\84)and serum androgen concentration (r = 0\m=.\96). The mean concentrations of l-carnitine, fructose, citrate and acid phosphatase for the two groups were not significantly different; but, related to the differences in ejaculate volumes, their total amounts in total ejaculate were lower in Group EP than in Group LP. These results suggest that, in chimpanzees, mechanisms of seminal plasma produc- tion and ejaculation are functional early in the reproductive life and that the emission of spermatozoa occurs later. Keywords: semen; chimpanzee; puberty; masturbation Introduction In humans, puberty is easily staged by the progressive appearance of characteristic physical signs (Tanner, 1962; Tanner & Whitehouse, 1976). In boys, growth velocity, penis and testis enlargement and pubic hair development are easily documented, but demonstration of sperm production remains difficult because of the ethical problems associated with semen collection (Richardson & Short, 1978; Hirsch et al, 1979, 1985). In male chimpanzees, the primate species most similar to man, external signs specific to puberty are not easily visible. However, several studies have emphasized a close resemblance between man and chimpanzee in terms of physical and hormonal changes at puberty (Gavan, 1953; McCormack, 1971; Martin et al, 1977; Watts & Gavan, 1982; Copeland et al, 1985). *Reprint requests to: Dr S. Meuris, Human Reproduction Research Unit, Hôpital Saint Pierre, 322, rue Haute, B-1000 Brussels, Belgium. Downloaded from Bioscientifica.com at 09/23/2021 08:49:53PM via free access In male chimpanzees in captivity, an increase in the rate of body weight gain starts at approximately 6-7 years of age, reaching an adult weight at 11-12 years of age (Spence & Yerkes, 1937; Grether & Yerkes, 1940; Smith et al, 1975). An increase in testis size is correlated with body weight increase during this period (Copeland et al, 1985), and testosterone concentrations also rise (McCormack, 1971; Martin et al, 1977). Stabilization of these measures and thus adulthood is reached at about 13 years of age (Smith et al, 1975). Although semen characteristics of adult chimpanzees have been described (Ackerman & Roussel, 1968; Roussel & Austin, 1968; Warner et al, 1974), there have been no studies of semen in the pubertal period. The purpose of the present study was to assess cellular and biochemical characteristics of semen in relationship to dental age, body weight, testicular volume and serum androgen in pubertal chimpanzees. Materials and Methods Animals. Six wild-born chimpanzees. Pan troglodytes troglodytes, were studied from May through August 1985. All were originally orphaned as infants by hunters and had been at the Centre International de Recherches Médicales de Franceville (CIRMF) for 4-6 years; each remained in excellent health throughout the study. The subjects were housed in large indoor-outdoor enclosures in age- and size-matched social groups of 4-6 chimpanzees of both sexes (except MG, who was caged with another male only). Their ages were estimated from regularly observed dental eruption since arrival at CIRMF (Nissen & Riesen, 1945, 1964). At 4-week intervals each animal was anaesthetized (between 09:00 and 11:00 h) by intramuscular injection of combined ketamine HC1 (Imalgène 1000, Rhône Mérieux, Lyon, France) and acepromazine maléate (Calmivet, Vetoquinol S.A., Lure, France) at dosages of 5-10 mg/kg and 0 5-0-10 mg/kg, respectively. Body weight was recorded and left testicular length (L) and width (W) were measured with Vernier calipers (Sade, 1964). Testicular volume (TV) was estimated using the formula: TV = Jtl/6W2L (Dixson et al, 1980). Blood samples were collected by venepuncture from a forearm vein. Sera were stored at 60°C until assayed. — Semen collection. The 6 animals were trained for semen collection by research workers. This was accomplished by attracting them to the bars of their enclosures with orange juice and grasping and stimulating the penis (usually already erect) with a gloved and lubricated hand. All subjects ejaculated within a maximum of 1 to 2 min. The entire ejaculate was collected into a sterile plastic flask. Collections were made from each subject once or twice a week between 08:00 and ll:00h. Semen analysis. Semen coagulated completely upon emission and all ejaculates were immediately incubated at 37°C for 1 h to obtain partial liquefaction. The volume of the liquefied fraction obtained was measured using a graduated pipette and sperm analyses were begun immediately. The remaining coagulum was weighed and then diluted (1 mg/ml) in Tyrode's solution containing 0-5% (w/v) trypsin type 1 (Sigma, St Louis, MO, U.S.A.) and incubated at 37°C (Hoskins & Patterson, 1967). Complete dissolution was reached within 30-60 min. The original volume of the coagulum was determined by subtracting the volume of Tyrode's solution added from the total volume obtained. Sperm analyses were performed separately on the spontaneously liquefied fraction and the trypsinized coagulum of each ejaculate as follows. (1) The percentage of motile spermatozoa was estimated by microscopic examination ( 400) of a 20-µ1 drop of semen placed between a slide and 22 32 mm coverslip. (2) The percentage of living spermatozoa (vitality) was assessed by the method of Eliasson (1977). A drop of semen was mixed with 2 drops of a saline solution containing 1% eosin Y (Sigma). After 30 sec, 3 drops of a saline solution containing 10% nigrosin (Sigma) were added. The mixture was then smeared and examined microscopically ( 400). The percentage of live (unstained) spermatozoa was determined from a count of 200 cells per smear. (3) Sperm counts were made in duplicate. Semen was diluted (1/20, 1/50, 1/100 or 1/200 according to sperm density roughly estimated by microscopic examination) in Ringer's solution containing 1% formaldehyde. The count was performed using a Thoma's haemocytometer and microscopic examination ( 400). (4) The percentage of morphologically normal spermatozoa was estimated according to the classification scheme proposed by David et al. (1975) for human spermatozoa. Spermatozoa were examined microscopically ( 1000) on a smear of each semen fraction stained with both Shorr's solution and haematoxylin-eosin. Seminal fluid biochemical analysis. After removal of samples for the sperm analyses, the remainder of each spontaneously liquefied fraction and trypsinized coagulum was centrifuged at 14 000 g for 10 min at room tempera¬ ture. The sperm-free supernatants were stored at 60°C until assayed. In some cases, the remaining volume was insufficient to perform the complete biochemical analysis— and the next semen sample obtained from the same animal was prepared and stored as above without sperm analysis except for the sperm count. To study the functional activity of the male genital tract, each of the following substances, L-carnitine, fructose, citrate and acid phosphatase, was measured in duplicate from the thawed supernatant of the liquefied fraction and the trypsinized coagulum of each semen sample. Downloaded from Bioscientifica.com at 09/23/2021 08:49:53PM via free access L-Carnitine was assayed using the method based upon the formation of 5-thio-2-nitrobenzoate anion from 5,5'-dithio¿«-nitrobenzoic acid (DTNB, Calbiochem, San Diego, CA, U.S.A.) as reported by Soufir et al. (1981). The assays were conducted on undiluted samples after deproteinization by centrifugation on CF 50 molecular filtration cones (Amicon, Danvers, NJ, U.S.A.) at 1000 g for 20 min at room temperature. The changes of absorbance were recorded at 405 nm on a Pye Unicam Kinetics spectrophotometer (Philips, Cambridge, U.K.). The sensitivity of the assay was of 20 nmol/ml. Fructose and citrate were assayed by enzymic methods (Bernt & Bergmeyer, 1974; Dagley, 1974) based on the change of absorbance at 334 nm due to reduction or oxidation, respectively, of nicotinamide coenzymes using kits purchased from Boehringer (Mannheim, West Germany). The assays were performed on deproteinized samples diluted 1/10 in distilled water for fructose and undiluted for citrate. The sensitivity of the assays was 15 mg/100 ml. Acid phosphatase activity was measured by colorimetry at 405 nm using para-nitrophenylphosphate as the substrate (PNP: Sigma) (Polakoski & Zaneveld, 1977). The assays were performed on samples diluted at 1/10 000 to 1/50 000 in distilled water Testosterone assay.
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