Ž .
Animal Reproduction Science 62 2000 297–307
www.elsevier.comrlocateranireprosci
Age-related changes in plasma testosterone
concentrations and genital organs content of bulk
and trace elements in the male dromedary camel
A.A. Al-Qarawi, H.A. Abdel-Rahman, M.S. El-Belely
),
S.A. El-Mougy
Department of Veterinary Medicine, College of Agriculture and Veterinary Medicine, King Saud UniÕersity,
P.O. Box 1482, Buraydah, Al-Qassim branch, Saudi Arabia
Received 8 October 1999; received in revised form 22 February 2000; accepted 20 March 2000
Abstract
There is a paucity of information regarding the influence of plasma testosterone concentrations and inorganic cations secreted in the different seminal fractions on the spermatozoon activity throughout the reproductive life of the one-humped camels. To demonstrate these relationships,
Ž . Ž . Ž
the genital organs of 12 prepubertal -3 years , 9 peripubertal 3–-5 years , 16 mature 5–-15
. Ž .
years and 15 aged G15 years camels were collected from the Buraidah slaughter house ŽAl-Qassim Province, Saudi Arabia during two consecutive breeding seasons November–April. Ž .
Ž .
over 2 years. Plasma testosterone concentrations mean"S.E. did not exceed 1.4 ngrml in
Ž .
prepubertal animals with a 3–4 fold increase in peripubertal 3.2"0.4 ngrml and mature Ž4.8"0.6 ngrml camels followed by about 50% decrease 2.6. Ž "0.3 ngrml in aged ones. These. hormonal changes were correlated significantly with concentrations of certain elements in the
Ž . Ž .
testes highest Na, Ca and Cu contents , epididymides highest P and Fe contents , prostrate Žhighest Zn content , and bulbo-urethral glands highest K and Mg contents . The significance of. Ž . some interrelationships among the different cations and their biological effects on sperm produc-tion and metabolic activity were discussed.q2000 Elsevier Science B.V. All rights reserved.
Keywords: Camel; Male reproduction; Testosterone; Testis; Epididymis; Prostate; Bulbo-uretheral gland; Bulk
and trace elements
)Corresponding author.
0378-4320r00r$ - see front matterq2000 Elsevier Science B.V. All rights reserved. Ž .
( ) A.A. Al-Qarawi et al.rAnimal Reproduction Science 62 2000 297–307
298
1. Introduction
It has been well established that the testes produces, in addition to androgens, considerable amounts of another type of secretion which flows from the lumina of the seminiferous tubules through the rete testes into the epididymides. Here a large part of the fluid is reabsorbed, but additional compounds are added as the spermatozoa pass down the epididymal duct. For most species, the spermatozoa remain immotile in the lower part of the epididymides and motility is activated when spermatozoa are mixed with secretions from different accessory glands during ejaculation.
Extensive studies on the distribution of organic and ionic components of semen Ž
between seminal fractions of many species Wallace and Wales, 1964; Quinn et al., . 1965; Wales et al., 1966; Setchell, 1974; Eissa et al., 1992; Hamamah and Gatti, 1998 were made to define its important effect on sperm motility and metabolic activity.
Ž . Ž .
Except for the reports by Abdel-Raouf and El-Naggar 1976 , Badawy et al. 1982 and Ž .
Abou-Ahmed et al. 1988 on the fructose and citric acid contents of the accessory glands, research pertaining to the role of the reproductive organs in producing various ionic compounds of the male camel could not be found in the available literature.
Ž .
The present study was, therefore, designed to: 1 investigate the concentrations of
Ž . Ž .
certain bulk Na, K, Ca, P and Mg and trace Zn, Cu, Fe elements in the testes, epididymides and accessory sex glands of the male dromedary camels throughout their
Ž .
reproductive life; 2 determine plasma testosterone concentrations to clarify how far differences in concentrations of these cations in the different reproductive organs are
Ž .
androgen dependent; and 3 compare the ion concentrations in all combinations to gauge the importance of possible interrelationships.
2. Material and methods
2.1. Samples collection and their assignment to groups
Blood as well as the external and pelvic genitalia of 56 clinically healthy, one-humped camels were collected from the Buraidah slaughter house during two consecutive breeding seasons. All samples used were grossly normal and free from pathological lesions. The camels were allotted to four groups according to their age. The age range in these groups was -3 years to over 15 years, according to the dentition formula given
Ž . by Rabagliati 1924 .
2.2. Chemical analyses
Ž .
Examination of specimens testes, epididymides, prostate and bulbo-urethral glands was conducted in the laboratory within 2–3 h after slaughter. The organs were first dissected from the surrounding fat and other tissues. Samples of known weight from
Ž .
()
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et
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Table 1
Ž . Ž . Ž . Ž . Ž .
Age-related changes means"S.E. in concentrations of plasma testosterone ngrml and bulk and trace elements mgr100 gm in the testes T epididymides E ,
Ž . Ž .
prostate gland P and bulbo-urethral glands B in camels
Group Age Testosterone Organ Na K Ca P Mg Zn Cu Fe
Žyears.
Prebupertal -3 1.1"0.1 T 1378.2"140.1 585.3"52.5 190.4"18.5 85.2"7.9 53.5"5.1 14.9"1.3 4.9"0.3 1.8"0.2
Žns12.
E 894.3"76.3 923.1"87.2 258.2"23.1 6824.1"670.1.1 69.2"6.3 10.5"0.8 5.6"0.5 3.2"0.3 P 1015.1"98.2 1985.4"180.1 169.2"15.1 74.5"7.3 43.6"3.8 189.1"17.6 3.2"0.2 2.7"0.2 B 1227.4"119.5 2468.2"231.3 148.1"13.9 166.3"15.5 84.2"7.6 97.3"9.8 2.1"0.9 1.6"0.1 Peribupertal 3–-5 3.2"0.4 T 5412.4"498.3 609.4"56.5 1425.3"136.2 718.6"70.1 58.3"5.4 26.4"2.2 5.8"0.6 1.5"0.1
Žns9.
E 2463.8"203.2 2506.1"240.3 659.4"61.7 8209.1"811.2 89.7"8.2 8.2"0.7 2.9"0.3 5.2"0.5 P 1119.5"101.1 4369.2"411.4 250.5"21.2 123.3"11.9 46.2"4.7 164.1"16.1 2.6"0.2 3.0"0.2 B 1364.8"129.7 5197.2"491.6 194.4"82.5 215.2"19.6 161.3"16.1 85.4"8.2 6.4"0.5 2.1"0.1 Mature 5–-15 4.8"0.6 T 5918.6"521.2 779.1"68.5 1765.1"161.3 884.3"73.2 49.1"3.8 31.5"2.8 2.6"0.2 1.3"0.9
Žns16.
E 3232.1"295.6 3168.4"281.3 711.6"63.3 8254.6"821.1 108.8"9.6 7.4"0.6 2.3"0.1 6.2"0.7 P 1207.3"118.5 4825.5"406.1 314.7"28.9 156.2"14.8 63.5"6.5 158.3"15.6 1.6"0.1 3.4"0.3 B 1394.8"128.7 5321.2"508.5 241.5"22.3 270.1"25.7 189.1"17.2 73.7"7.2 3.1"0.2 2.5"0.3 Aged G15 2.6"0.3 T 3425.7"321.1 1168.7"96.6 3553.1"341.2 662.9"58.3 40.3"3.8 22.4"2.7 3.1"0.2 2.3"0.2
Žns15.
E 1556.4"148.5 1354.2"121.4 2118.3"193.5 3094.5"28.9 73.5"7.2 12.6"1.5 3.4"0.3 5.0"0.6 P 1005.8"96.9 2118.3"184.1 715.8"69.2 93.5"8.6 50.2"4.4 231.8"22.5 4.2"0.3 3.1"0.3 B 1116.5"107.3 2206.2"201.1 576.1"52.7 142.7"13.4 134.8"13.1 125.3"11.8 3.0"0.2 2.2"0.2 Overall -3–15 3.1"0.2 T 4033.2"128.4 785.7"63.8 1733.5"84.4 587.3"146.2 50.0"4.2 23.3"1.9 5.3"0.5 1.7"0.2
Žns52.
()
The interaction of age, plasma testosterone concentrations and mineral contents of testes T , epididymides E , prostate gland P and bulbo-urethral glands B in camels
Parameters Testosterone Organ Na K Ca P Mg Zn Cu Fe
) ) ) ) ) )
Age 0.281 T 0.301 0.273 0.873 0.277 y0.108 0.203 0.104 y0.213
) ) ) ) ) )
E 0.275 0.280 0.625 0.283 0.282 0.087 0.116 y0.169
) ) ) ) ) ) ) )
P 0.286 0.324 0.731 0.291 0.298 y0.511 0.095 y0.200
) ) ) ) ) ) ) )
B 0.270 0.351 0.814 0.315 0.291 y0.407 0.086 y0.185
) ) ) ) ) ) ) ) ) )
Testosterone T 0.735 0.526 y0.309 0.170 0.183 0.406 0.310 y0.392
) ) ) ) ) ) ) ) )
E 0.681 0.613 y0.276 0.614 0.309 0.125 y0.299 0.207
) ) ) ) ) ) ) ) ) ) )
P 0.813 0.414 y0.313 0.078 0.518 y0.552 y0.316 0.295
) ) ) ) ) ) ) ) ) ) )
B 0.625 0.379 y0.325 0.084 0.463 y0.433 y0.303 0.304
) ) ) )
Na T y0.485 0.063 y0.139 0.166 y0.325 0.061 0.274
) ) ) )
E y0.516 0.088 y0.202 0.148 y0.291 0.144 0.318
) ) ) )
P y0.296 0.126 0.081 0.212 y0.420 0.088 0.296
) ) )
B y0.324 0.050 0.056 0.205 y0.311 0.054 0.355
) ) ) )
K T 0.022 0.111 0.206 0.465 0.300 y0.351
) ) ) ) )
E 0.011 0.053 0.181 0.518 0.312 y0.401
) ) )
P 0.035 0.104 0.210 0.299 0.290 y0.329
) ) )
( ) A.A. Al-Qarawi et al.rAnimal Reproduction Science 62 2000 297–307
302
furnace for another 3–4 h after adding a few drops of concentrated nitric acid. The ash content of each sample was placed in a dry clean vial, dissolved in 0.5 N nitric acid with a final volume of 7 ml and analyzed at the end of the season.
Na and K concentrations were assayed by emission flame photometry, whereas Ca, Zn, Cu and Fe were determined using atomic absorption spectrophotometry as described
Ž . Ž . Ž .
by Clegg et al. 1981 . P Bio-Merieux, France and Mg Bayer diagnostics, Germany were determined colorometrically using commercial kits.
2.3. Hormonal analysis
Jugular blood was collected after slaughtering into EDTA-containing vials, cen-trifuged at 1500 g for 20 min. Plasma was stored aty608C pending hormonal assays. The concentration of testosterone was measured in duplicate in 200 ml of plasma
Ž .
without column separation from dihydroxytestosterone DHT using a method previ-Ž .
ously described by El-Belely et al. 1995 . The cross-reactivity of the antibody was 100% testosterone, 58.6% 5 a-DHT, 54.3% 5 b-DHT, 15.6% androstenedione, 7.8% corticosterone, and less than 1% oestriol and oestradiol 17a. The sensitivity of the assay was 10 pgrml. The average intra- and inter-assay coefficients of variation in six assays were 13.5% and 14.2%, respectively.
2.4. Statistical analyses
Changes in plasma testosterone concentrations and mineral contents of different genital organs within and between age groups were statistically evaluated by the least
Ž .
squares analysis of variance using the general linear models GLM procedures of the
Ž .
statistical analysis system SAS, 1996 . Correlations between hormonal and mineral concentrations were undertaken using SAS procedures.
3. Results
The age related changes in concentrations of plasma testosterone and bulk and trace elements in the testes, epididymides and accessory glands are shown in Table 1.
Plasma testosterone concentrations increased progressively with age advancement,
Ž . Ž .
reaching its highest values mean"S.E. in the mature 4.8"0.6 ngrml compared to
Ž . Ž . Ž
prepubertal 1.1"0.1 ngrml , peripubertal 3.2"0.4 ngrml and aged 2.6"0.3 ng .
rml camels.
Ž
The overall mean values of the studied minerals revealed that Na 4033.4"128.2
. Ž . Ž .
mg% ; Ca 1733.5"84.4mg% and Cu 5.3"0.5mg% were more concentrated in the
Ž . Ž .
testes. The higher concentrations of P 6595.8"511.6 mg% and Fe 4.9"0.4 mg% were found in the epididymides. Prostate gland had the highest concentration of Zn Ž185.5"16.3 mg% , whereas bulbo-urethral gland contained the highest concentration.
Ž . Ž .
of K 3798.4"253.2mg% and Mg 141.1"30.5mg% .
concentra-( )
A.A. Al-Qarawi et al.rAnimal Reproduction Science 62 2000 297–307 303
tions in the prostrate and bulbo-urethral glands of the peripubertal as compared to prepubertal animals. There was a further, though less marked, increase in Na and K
Ž .
contents in all genital organs of the mature camels followed by dramatic P-0.01 decreases in both elements in those of the aged animals. As a result of these changes in the distribution of Na and K, the Na to K ratio changed from about 2:1 in the testes and accessory glands of those in the prepubertal age to about 9:1 in the testes and 1:4 in the accessories of peripubertal and mature animals. These ratios changed to 3:1 and 1:2, respectively, in these organs of animals over 15 years old. The ratios of both electrolytes changed to a little over 1:1 in the epididymides of the latter camels. Moreover, the genital organs of these animals contained 2 to 3 times greater Ca and Cu contents than found in those of the peripubertal and mature animals. The reverse was found true
Ž .
concerning P, Mg and Fe, particularly the marked decrease P-0.01 in testicular Mg, epididymal P and Fe in the aged dromedaries. Concentration of Zn displayed a different
Ž .
pattern where testicular content decreased P-0.05 whilst epididymal and accessories
Ž .
content increased P-0.01 in the aged compared to young and mature animals. The interaction between plasma testosterone and minerals studied are shown in Table 2.
Concentrations of plasma testosterone were correlated significantly with the content of Na, K, Ca and Mg in all genital organs but only with epididymal content of P and with the content of Zn in the accessory glands. Correlations between the content of the different bulk and trace elements in all genital organs included significant positive correlations between Na and Fe as well as between Zn and Cu; and significant negative correlations between Na and each of K and Zn, Ca and each of P and Mg and between Zn and Fe as well as Cu and Fe.
4. Discussion
Ž
The present study demonstrated that detectable levels of plasma testosterone 1.1"0.1 .
ngrml were found in all samples beginning at 2.4"0.2 years, increasing steadily to 4.8"0.6 ngrml up to 8.2"0.2 years and remained fairly constant until 13.6"1.6
Ž .
years followed by a marked decline 2.6"0.3 ngrml afterwards. From these data, it
Ž .
appears that plasma testosterone concentrations peaked 6.4"0.7 ngrml at 5.8"0.7 years, which is when sexual maturity is reached. These findings approximated those reported in different animal species but with earlier initiation of testosterone secretion at not more than 6–8 months and peaking at around 36 months old as reported in bulls ŽBedaire and Thibier, 1979; Lacroix and Pelletier, 1979; Amann and Walker, 1982;
. Ž . Ž .
Amann, 1983 , stallions Pickett et al., 1981 and boars Gray et al., 1971 .
( ) A.A. Al-Qarawi et al.rAnimal Reproduction Science 62 2000 297–307
304
Ž
micropuncture contained more Na and less K than epididymal fluid Wallace and Wales, .
1964; Quinn and White, 1966; Setchell, 1974 and that K concentrations greatly
Ž .
exceeded Na in their accessory secretions Quinn et al., 1965; Eissa et al., 1992 . In contrast to the present findings that testes, and to a lesser extent, epididymides contained more Ca than did accessories, the bulk of Ca in the ejaculated bull semen
Ž .
comes chiefly from the seminal vesicles Quinn et al., 1965; Eissa et al., 1992 . The finding that epididymal P concentration was almost 10 times as high as that in testes and 50–60 times greater than that in accessories may be accounted for by
Ž .
increasing levels of glycerylphosphorylcholine Wales et al., 1966; Crabo et al., 1967 . However, these authors reported P concentration in bull and ram epididymides about one-third the concentration found in camel leading to the conclusion that camel spermatozoa might utilize large amounts of glycerylphosphorylcholine in the female genital tract.
The present results indicated that all genital organs contribute to the Mg content of seminal plasma. However, as with K, higher Mg concentrations were detected in
Ž . Ž .
samples from bulbo-urethral gland. Wallace and Wales 1964 , Quinn et al. 1965 and Ž .
Eissa et al. 1992 reported in bulls a rather high Mg content secreted mainly from seminal vesicles.
Among the chemical peculiarities of the male genital organs of camels is the rather high content of Zn. The prostate gland was strikingly rich in these elements, the concentration of which reached levels almost 7–8, 18–20 and 2–3 times higher than in the testes, epididymides and bulbo-urethral glands, respectively. Earlier studies in man showed that the prostate gland is characterized by its capacity to concentrate Zn ŽNawson and Fisher, 1951; Gyorkey et al., 1967; Bronner and Coburn, 1981 in amounts.
Ž .
greater than do other tissues such as testis, brain or blood Vallee, 1962; Mann, 1962 . A Ž
high level of Zn is equally characteristic of the bovine Gawthorne et al., 1982; Eissa et
. Ž . Ž .
al., 1992 , canine Whitmore, 1963 and rat Gunn et al., 1955 prostate.
Our findings revealed that Cu was highly concentrated in the testes, more than so in other genital organs, but there was notably more Fe in the epididymides. These findings
Ž . Ž .
differ from those found in bulls by Quinn et al. 1965 and Eissa et al. 1992 , which reported that both elements were highly concentrated in the accessory glands.
The present marked changes in the bulk and trace elements in different genital compartments due to age seem to be governed primarily by the associated changes in plasma testosterone concentrations. The marked increase in this steroid during the pubertal and mature ages was associated consistently with an increase in the content of Na, K, Ca, P and Zn of the genital organs. The marked decline in those minerals in the aged camels paralleled the marked decline in plasma testosterone concentrations. In
Ž . Ž
confirmation, the excision of testes in adult bull Eissa et al., 1992 , boar Joshi and
. Ž . Ž
Raeside, 1973 , dog Barron and Huggins, 1944 and rat Rudolph and Starnes, 1954; .
Butler and Schade, 1958 resulted in a rapid reduction of the weight of accessory glands together with their diminished capacity to produce fructose and citric acid. Moreover, treatment of castrated boars increased the secretory activity of these glands from the levels in the pre-castration periods.
Table 2 revealed some interesting correlations between cation levels in the genital
Ž .
( )
A.A. Al-Qarawi et al.rAnimal Reproduction Science 62 2000 297–307 305
Ž .
of accessory organs low Na and high K are in agreement with earlier reports in bulls
Ž .
and rams Cragle et al., 1958; Dott and White, 1964; Quinn and White, 1966 . These investigators observed high Na and low K in the testicular fluid and the ratio between them is reversed in seminal plasma secreted by the accessory glands. The reciprocal
Ž relationships between Ca and each of P and Mg in the testes and prostate gland high
. Ž
Ca, low P and Mg and the epididymides and bulbo-urethral gland low Ca, high P and
. Ž .
Mg were observed in humans by Gawthorne et al. 1982 who reported that an increased uptake of Ca by different tissues caused a reduction in the retention rate of the other two elements by these tissues. The finding that Zn and Cu were positively
Ž .
correlated in all genital organs of camels is at variance with Rose 1981 who found that supplementation of pregnant women with large amounts of Zn led to Cu deficiency. However, the author fed amounts of Zn in excess of the recommended dietary allowance. The interaction between Zn and Fe as revealed by the low Zn and high Fe in the testes and epididymides with the reversed relationships between those of the
Ž .
accessory glands supported the view of Momcilovic 1982 that the specificity of Zn binding ligands was impaired in the presence of adequate amounts of Fe. He also added that Fe absorption increased in animals, including man, fed Cu deficient diet which is in parallel with our results that higher concentrations of Cu in the testes and accessory organs is associated with reduced Fe concentration in these organs.
The present study could suggest that concomitant with the marked decline in plasma testosterone concentrations, the mechanisms controlling normal cation distribution in the testes, epididymides and accessory glands are clearly disturbed in the aged camels. This might provide an explanation for the reduced gonadal sperm reserve, the increased percentage of spermatozoal abnormalities and the poor axonemal motility characteristic
Ž
of semen collected from aged camels Singh and Bharadwaj, 1978; Tingari et al., 1986; .
Wilmen et al., 1993 .
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