The frontal and gular dermal scent organs of the marsupial sugar glider (Petaurus breviceps)

A study spanning two breeding seasons was carried out to examine the role of androgens in the control of the frontal and gular scent glands of the marsupial sugar glider Petaurus breviceps Waterhouse in a wild population. Animals were captured at monthly intervals and from these blood samples were taken and tissue biopsy samples were collected from the scent glands.
Several histological parameters underwent seasonal changes which were related to changes in the plasma concentration of free plus albumin bound ('biologically active') testosterone. The parameters which showed significant change did so during the July-September breeding season coinciding with the peak in biologically active testosterone concentration.
Castration caused a significant decrease in the nuclear diameters of gular and frontal apocrine and sebaceous gland cells, and a decrease in gular apocrine cell height. These decreases were reversed with androgen replacement therapy.
The nuclear diameters of apocrine tissue cells in both scent organs are positively correlated with the plasma level of biologically active testosterone. In the gular organ, but not in the frontal organ, the depth of apocrine tissue was significantly correlated with nuclear diameter. In castration and androgen replacement studies gular apocrine tissue responded more dramatically than did frontal apocrine tissue. This suggests that the gular organ is more sensitive to testosterone than is the frontal.     

Seasonal timing of sperm production in roe deer: interrelationship among changes in ejaculate parameters,morphology and function of testis and accessory glands

Roe deer are seasonal breeders with a short rutting season from mid-July to mid-August. The seasonality of reproductive activity in males is associated with cyclic changes between growth and involution of both testes and the accessory sex glands. This study characterizes morphological and functional parameters of these organs prior to, during and after breeding season in live adult roe deer bucks. Size and morphology of the reproductive tract was monitored monthly by transcutaneous (testes, epididymis) and transrectal (accessory glands) ultrasonography. Semen was collected by electroejaculation. Concentration, motility and morphological integrity of spermatozoa as well as the content of proteins and testosterone in semen plasma were evaluated. Proportions of haploid, diploid and tetraploid cells were estimated by flow cytometry in testicular tissue biopsies. Serum testosterone was measured by enzyme immunoassay. Most parts of the male reproductive tract showed distinct circannual changes in size and texture. These changes were most pronounced in the testes, seminal vesicles, and prostate. All reproductive organs were highly developed during the rut only. The volume of ejaculates, total sperm number and percentages of motile and intact spermatozoa also showed a maximum during this period and corresponded with high proportions of haploid cells in the testis. The highest percentages of tetraploid cells were found in the prerutting period. The production of motile and intact spermatozoa correlated with both the protein content of semen plasma and the concentration of testosterone in semen plasma and blood serum. These results suggest the importance of combined actions of the testes and accessory sex glands and the crucial role of testosterone in facilitating the optimal timing of intensified semen production to ensure sufficient numbers of normal spermatozoa in seasonal breeders.     

Central and peripheral action of testosterone propionate on scent gland morphology and marking behaviour in the Mongolian gerbil

Scent gland size and activity and frequency of marking under standard conditions were compared in five groups of male and female gerbils: (1) intact, sham-operated controls, (2) intact with scent glands excised, (3) gonadectomized, (4) gonadectomized injected with 1000 μg testosterone propionate (TP) on alternate days, and (5) gonadectomized with a low dose (25 μg) TP applied topically to the ventral scent gland on alternate days. The animals were housed in individual cages and tested for marking in an open field arena with plastic pegs.The scent gland is not required in either sex for the behavioural act of marking. Topical application of a dose of TP too low to exert a systematic effect restored the scent gland but not marking. Injection of sufficient TP to restore seminal vesicle weight restored marking, as well as the scent glands.It was concluded that in the male, both marking behaviour and scent gland size are controlled by the testes. The effect of androgens on marking is mediated directly through the central nervous system, and not through peripheral stimulation of the glands.Females have smaller glands and mark less than males. The ovaries appear to have little control over marking frequency, and some control over scent gland size. It is possible to stimulate marking behaviour to supernormal levels by TP injection, but not by topical application.     

A study of seasonally delayed puberty in the male hare, Lepus Europaeus.

The brown hare, Lepus europaeus, has a mating season which extends from January to September. Adult males exhibit pronounced seasonal changes in the reproductive tract which are associated with changes in LH secretion. Maximum plasma levels of immunoreactive LH occur between March and June and minimal levels in the autumn non-mating period from September to December; this seasonal cycle in gonadotrophin output is reflected by the appropriate changes in the secretion of testosterone from the testes and in the activity of the accessory sex glands. Juvenile animals reach puberty only during the adult mating season, and the age of puberty thus varies with the date of birth. Males born before May reach puberty and become fertile at 3 months of age, while those born from May to July grow to a mature body size during the autumn non-mating season but puberty is delayed for several months. Since some animals experiencing delayed puberty were found to have elevated plasma levels of LH and testosterone, it is concluded that puberty is not completely suppresed by the environmental effects of the autumn, but that the developmental process is prolonged, resulting in the juveniles being synchronized with the adults in their reproductive activity.     

Age-related changes on marking, marking-like behavior and the scent gland in adult Mongolian gerbils (Meriones unguiculatus).

Marking behavior, marking-like behavior [3], and changes of the scent glands were observed in aged Mongolian gerbils. In Experiment 1, changes in the marking and marking-like behavior with aging were evaluated in adult male and female Mongolian gerbils of an inbred strain aged 6 to 36 months. The frequency of marking behavior in males was significantly higher than females throughout the observation period except at 36 months of age. On the other hand, frequency of marking-like behavior in males, but not in females decreased with aging, significantly. In Experiment 2, changes of the scent gland in adult males and females aged 6 to 36 months were morphologically evaluated. Macroscopic examination revealed an increase in the size length and width of the glands of males aged 12 months and females aged 6 months. Histologically the glands of all the males and females aged 6 months developed moderately or well. Some of the 12-month-old males and females showed acinar atrophy of the glands, and all the females aged 18 months or more had highly atrophied scent glands. From these results, we concluded that there is no relationship between the changes of marking behavior and those of the scent glands in aged male Mongolian gerbils, and assume that marking behavior in aged animals does not have an important meaning as marking. In Experiment 3, marking and marking-like behavior in castrated adult Mongolian gerbils aged 16 weeks were observed. The result showed that marking behavior, not marking-like behavior was inhibited after castration. From these findings, we consider that generally marking behavior in Mongolian gerbils consists of androgen-dependent marking behavior and androgen-independent marking behavior (marking-like behavior).     

Lack of gonadal control of the dorsal gland and sandbathing in male and female bannertail kangaroo rats (Dipodomys spectabilis)

Previous studies have demonstrated gonadal control of mammalian scent glands; castration leads to reduced scent-marking rates and smaller gland sizes. I investigated whether gonadal hormones control the size of the dorsal gland (a specialized sebaceous gland) and sandbathing as a scent-marking behavior in adult male and female bannertail kangaroo rats (Dipodomys spectabilis). Gland sizes of males and females were similar in all age classes, except adult males with larger body weights had proportionately larger glands than females. Male gland sizes declined 18% following castration but were not significantly smaller than those of intact males; females showed no change in dorsal gland size either as a result of ovariectomy or after estradiol benzoate implants. Sandbathing rates also did not decline as a result of gonadectomy. Rather, castrated males and overiectomized females sandbathed at higher frequencies than intact males and ovariectomized females with estradiol benzoate implants, respectively. Gonadal hormones apparently have little influence on the function of a specialized scent gland and may inhibit sandbathing as a scent-marking behavior in adult D. spectabilis.     

Neuroendocrine response to female ovulatory odors depends upon social condition in male common marmosets, Callithrix jacchus

Male mammals show rapid behavioral and hormonal responses to signals from sexually receptive females. However, rapid endocrine responses to female signals have not been observed in a nonhuman primate. Here, we tested the behavioral and hormonal response of male common marmosets (Callithrix jacchus) to isolated scent secretions from ovulatory females or to vehicle control scent. Fifteen males were tested in their home cage for behavioral and hormonal responses. These males showed increased investigative and arousal behaviors to the ovulatory scent compared to the vehicle scent. Time sniffing the scent substrate and the duration of erections were significantly elevated in relation to the vehicle scent. Thirty minutes after presentation of ovulatory scent, males showed a significant increase in testosterone compared to the vehicle, but there was no difference in cortisol values. To better control for scent presentation, 15 additional males were tested under a controlled scent exposure. Current social housing condition influenced the male's testosterone response to the ovulatory scent. Single and paired males showed significant increases in testosterone levels with the ovulatory scent but did not increase cortisol levels. Single males also showed the highest change in testosterone with the ovulatory scent, but fathers showed no changes. These results indicate that a rapid hormonal response to sexually arousing cues occurs in marmosets, and the data suggest that a male's social condition influences how he responds to sexually relevant cues.     

Testosterone-dependent primer pheromone production in the sebaceous gland of male goat

To test the hypothesis that the primer pheromone responsible for inducing the "male effect" is produced in the sebaceous gland androgen dependently, we examined the correlation between morphological changes of sebaceous glands and the pheromone activity in skin samples taken from castrated goats that had been treated with testosterone. Five castrated goats were implanted s.c. with testosterone capsules to maintain physiological levels of plasma testosterone for four weeks. Skin samples were obtained from the head region on Day 0 (the day of testosterone implant), Day 7, Day 14, Day 28 (the day of testosterone removal), Day 36, Day 42, and Day 56. Matched blood samples were also collected for measurement of testosterone concentration. The pheromone activity of the ether-extracts of the upper dermal layer containing sebaceous glands was assessed by its stimulatory effect on the hypothalamic GnRH pulse generator, which was monitored for changes of specific multiple unit activity (MUA) in ovariectomized estradiol-primed goats as described previously. The sebaceous gland enlarged during the testosterone treatment but reduced in size after testosterone removal. The pheromone activity first appeared in 2 out of 5 goats on Day 7 and in all the 5 goats by Day 28. Fourteen days after testosterone removal (Day 42), the pheromone activity was no longer detectable in any of the 5 goats. In short, the sebaceous gland size and the pheromone activity shifted almost in parallel. The present results provide strong support for the view that the primer pheromone is produced testosterone dependently in the sebaceous gland of the male goat.     

Histological examinations of facial glands in <Emphasis Type="Italic">Saccopteryx</Emphasis><Emphasis Type="Italic">bilineata</Emphasis> (Chiroptera,Emballonuridae), and their potential use in territorial marking

Scent marking is widespread among individuals of Mammalia species, especially in resource defence social systems. Apart from urine and faeces that are used for claiming resource ownership, specialised scent glands are the main source of secretions in scent marking individuals. Most previous studies have described secretory epithelia macroscopically, since many glands are conspicuous. But macroscopically inconspicuous scent glands or morphological structures might then be overlooked. In Saccopteryx bilineata (greater sac-winged bat), behavioural observations suggest that both sexes have, apart from the conspicuous gular glands of males, specialised facial glands to display territorial marking. We investigated the facial glands of two males and one female S. bilineata histologically and found, first, that both sexes possess a bilateral symmetrically intermandibular gland, which is composed of a bed of modified apocrine sudoriferous cells. Second, we found lip glands consisting of modified apocrine sudoriferous cell units with pigmented ducts around the upper and the lower lip. Both gland types are probably involved during territorial marking.     

Horn growth related to testosterone secretion in two wild Mediterranean ruminant species: the Spanish ibex (Capra pyrenaica hispanica) and European mouflon (Ovis orientalis musimon)

Seasonal variations in the horn development and testicular activity of the Spanish ibex (Capra pyrenaica hispanica) (n=6) and European mouflon (Ovis orientalis musimon) (n=5) were monitored to determine the role of increasing testosterone concentration on the arrest of horn growth during the rutting season. Marked seasonal variations in the rate of horn growth (P<0.01) and testicular activity (P<0.001) were seen in both species, although the magnitude and timing of these changes were different (P<0.01). Horn growth rate was inversely correlated to seasonal levels in testosterone plasma concentration in both species (ibex: R=-0.45, P<0.01; mouflon R=-0.51, P<0.01). In the mouflon, the increase in plasma testosterone concentration recorded in September (P<0.05 compared with the lowest concentration) coincided with a significant reduction in horn growth (P<0.05). In the ibex, the increase in plasma testosterone concentration in October (P<0.05 compared with the lowest concentration) was associated with a significant arrest of horn growth in November (P<0.05). These results appear to support the hypothesis that high peripheral plasma levels of testosterone are linked with the seasonal arrest of horn growth during the rutting period.     

Seasonal and developmental changes of reproductive organs of male ringed seals (Phoca hispida) in the Svalbard area

The weights of testes, prostate gland and baculum of ringed seal males were related to age, season and differences in body size. There was a significant seasonal variation in testes and prostate gland size of sexually mature males, with a maximum occurring in early April. There were no seasonal changes in prostate weight of immature males, but some of the older immatures had elevated testes weights in April. Testes weight was significantly correlated with lean body mass. The increase in testes size with increasing body weight was greater for seals six years of age or older than for younger males. We suggest that some testicular growth and a seasonal cycle in testes growth occur before the testes become functional endocrinologically. We also believe that the primary event leading to puberty in ringed seals is an age-dependent shift in metabolic processes, directing a larger percentage of available energy towards the reproductive organs.     

Testicular and androgen dependence of skin gland morphology in the anurans,Xenopus laevis and Rana pipiens

In anuran amphibians, there is increasing evidence that exocrine glands dispersed throughout the general integument are secondary sex characters (SSC). Following the recent discovery of sexually dimorphic “breeding glands” in the dorsum of male Rana pipiens, we studied the effects of castration and testosterone treatment on the dorsal skin glands of male Xenopus laevis and R. pipiens to determine whether the dorsal breeding glands, or any other dorsal skin glands, are androgen dependent. The dorsal skin glands of X. laevis were unaffected by androgen status. By contrast, in R. pipiens, breeding, mucous, and seromucous glands responded to testosterone stimulation. Mucous glands were significantly (P < 0.05) larger in testosterone-treated frogs than in castrates. There was a large, but statistically insignificant, increase in the size of the dorsal breeding glands. Testosterone treatment also increased the epithelial cell height of breeding and seromucous glands (P < 0.05). In the skins of castrated and testosterone-treated frogs, there was a reciprocal relationship between the abundance of seromucous and breeding glands: in castrates, seromucous glands were abundant and breeding glands virtually absent, whereas in testosterone-treated frogs, breeding glands were abundant and seromucous glands less common. The total number of the two gland types was similar in both treatment groups. Glands that appeared to be intermediate in form between seromucous and breeding glands were observed in some frogs. These data suggest that seromucous glands may be the regressed form of breeding glands in the dorsal skin of R. pipiens and that the dorsal skin of R. pipiens is a SSC. © 1993 Wiley-Liss, Inc.     

Observation of marking-like behavior, marking behavior, and growth of the scent gland in young Mongolian gerbils (Meriones unguiculatus) of an inbred strain.

A marking-like behavior (defined by authors), a marking behavior, and growth of the scent glands were observed in young Mongolian gerbils of an inbred strain. In males and females, a marking-like behavior, in which animals rub their abdominal scent glands on the floor, began to be seen at the age of 19 days and could be seen in almost all the gerbils at 22 days of age during the suckling period. The frequency of this behavior was highest at 60 days of age (males: 17.9/10 min, females: 15.4/10 min) and there was no sex difference. Marking behavior, in which animals rub their abdominal scent glands on small protruding objects, began to be seen at the age of 40 days in males and 50 days in females. The frequency of this behavior tended to increase until 90 days of age in males (13.7/10 min), but the levels were low (2.5-5.0/10 min) in females. The values in the male group therefore tended to be higher than that in the female group. Macroscopic scent gland pads were clearly observed at the age of 30 days in males, but not until 45 days of age in females. At the age of 45-90 days, the length of the scent gland pad in males and females was 2.1-2.8 and 1.6-1.7 cm, respectively and the width was 0.3-0.5 in males and 0.2-0.3 cm in females. During this period, the length and depth of the pads in males were significantly greater than those in females (p < 0.05). Histological examination of the structure of the scent glands after the age of 45 days showed that the development of clusters of acinar cells in females occurred much later than that in males, but the basic structure of these glands was similar in both sexes. These results suggest that the marking-like behavior was manifested although during the period when the scent glands had not yet developed, whereas true marking behavior first occurred when the glands were moderately well developed.     

Seasonal variation in reproductive physiological status in the Iberian ibex (Capra pyrenaica) and its relationship with sperm freezability

The present work examines the relationship between seasonal changes in testicular function, accessory gland size, and horn growth in Iberian ibexes, as well as the relationship between these changes and the resistance of ibex spermatozoa to freezing-thawing. The size of the bulbourethral glands and seminal vesicles showed pronounced monthly variation (P < 0.001), which was correlated positively with the plasma testosterone concentration (P < 0.001) and scrotal circumference (P < 0.001). The size of the accessory sex glands peaked during the autumn. Overall, semen quality was markedly improved during autumn and winter. When horn growth was at a minimum during autumn and winter, semen quality and accessory gland size were all increased compared to in spring and summer. However, increased plasma testosterone levels in the autumn were strongly associated with reduced sperm freezability; thus, the cryosurvival of spermatozoa collected during the autumn was poorer than at other times of the year. In winter, however, when the plasma testosterone concentration fell to baseline, the negative effects of cryopreservation on the percentage of motile spermatozoa and on the integrity of the plasma membrane of frozen-thawed sperm cells were significantly less intense (P < 0.05). These findings show a clear relationship between the functional and morphological status of the different parts of the reproductive tract that optimises reproductive function during the breeding season in the ibex male. They also show that winter is the most suitable season for the collection and cryopreservation of ibex spermatozoa.     

Seasonal variation in reproductive physiological status in the Iberian ibex (Capra pyrenaica) and its relationship with sperm freezability

The present work examines the relationship between seasonal changes in testicular function, accessory gland size, and horn growth in Iberian ibexes, as well as the relationship between these changes and the resistance of ibex spermatozoa to freezing-thawing. The size of the bulbourethral glands and seminal vesicles showed pronounced monthly variation (P < 0.001), which was correlated positively with the plasma testosterone concentration (P < 0.001) and scrotal circumference (P < 0.001). The size of the accessory sex glands peaked during the autumn. Overall, semen quality was markedly improved during autumn and winter. When horn growth was at a minimum during autumn and winter, semen quality and accessory gland size were all increased compared to in spring and summer. However, increased plasma testosterone levels in the autumn were strongly associated with reduced sperm freezability; thus, the cryosurvival of spermatozoa collected during the autumn was poorer than at other times of the year. In winter, however, when the plasma testosterone concentration fell to baseline, the negative effects of cryopreservation on the percentage of motile spermatozoa and on the integrity of the plasma membrane of frozen-thawed sperm cells were significantly less intense (P < 0.05). These findings show a clear relationship between the functional and morphological status of the different parts of the reproductive tract that optimises reproductive function during the breeding season in the ibex male. They also show that winter is the most suitable season for the collection and cryopreservation of ibex spermatozoa.     

Seasonal cycles in testicular activity in Mouflon, Soay sheep and domesticated breeds of sheep: breeding seasons modified by domestication

The seasonal reproductive cycle in rams was monitored in Mouflon (wild-type), Soay (feral type) and a variety of domesticated breeds of sheep (Shetland, Blackface, Herdwick, Norfolk, Wiltshire, Portland and Merino) by measuring the changes in the diameter of the testes (first three years of life in all breeds) and the blood plasma concentrations of FSH and testosterone (first four to six years of life in Mouflon and Soay rams). In the Mouflon rams there was a pronounced seasonal cycle in all the reproductive parameters from one to six years of age. The plasma concentrations of FSH increased from June to September associated with redevelopment of the testes; maximum testicular size and plasma concentrations of testosterone occurred in October at the onset of the rut. In the Soay and domesticated breeds the seasonal maximum in testicular size occurred in late September or October except in two of the southern breeds (Portland and Merino) which showed an earlier peak to the sexual cycle in August. The change in size of the testes from the minimum to the maximum was less in the domesticated breeds (135–157%) compared to the Soay (171%) and Mouflon (160%). Crossbred rams produced by mating Soay ewes (highly seasonal breed) with Portland or Merino rams (less seasonal breed) had a seasonal testicular cycle intermediate in timing compared to the pattern characteristics of the parent breeds; this is consistent with the involvement of multiple genes in the mechanism controlling the sexual cycle in the ram. The earlier seasonal onset of full testicular activity in the southern breeds is assumed to be the result of selection for a prolongation of the breeding season for early lambing.     

Differential effects of short photoperiod on the release of progesterone and testosterone by hamster testes in vitro

Suppression of testicular activity in hamsters and voles exposed to constant darkness or short photoperiod is associated with reduced ability of the testes to convert C21 steroid precursors to C19 androgens. In the present study, we have examined the time course of changes in testicular secretion of progesterone and testosterone in vitro in adult male golden hamsters exposed to short photoperiod. Gradual decrease in testicular weight after 1, 2, and 3 months of exposure to short photoperiod was accompanied by significant increase in the amount of progesterone released per milligram of testicular tissue in response to gonadotropin stimulation. In contrast, testosterone response to gonadotropic stimulus progressively decreased. These results suggest that photoperiod-related gonadal atrophy may be accompanied by reduced activity of the 17 alpha-hydroxylase: C17,20-lyase enzyme complex in the testes, and that seasonal transitions between the states of reproductive activity and quiescence involve changes in both the amount of steroids produced by the testes and the relative proportions of testosterone and its precursors.     

Vitamin D3 (soltriol) nuclear receptors in abdominal scent gland and skin of Siberian hamster (Phodopus sungorus) localized by autoradiography and immunohistochemistry

In vivo autoradiography with [³H]1,25-dihydroxycholecalciferol (vitamin D, soltriol) and immuno-staining with antibodies to vitamin D receptor were applied to identify specific binding sites in the abdominal scent gland of male Siberian hamster (Phodopus sungorus). Nuclear concentration of radiolabeled hormone and receptor antibodies was observed in the corresponding cell types including basal cells of sebaceous glands, cells of the outer hair sheaths and hair bulbs, and also keratinocytes in the epidermis. Cells of the hair dermal papillae and fibroblasts of the dermis did not show nuclear labeling. There was good correspondence between the autoradiographic and immunohistochemical data. The results indicate the presence of receptors for vitamin D-soltriol and suggest a seasonal regulation of scent gland marking activities by this steroid hormone of sunlight in cooperation with the sex steroid testosterone.     

Correlates of testis mass in capybaras (Hydrochaeris hydrochaeris): dominance assurance or sperm production?

To infer possible functions for the low gonadosomatic index and the high proportion of non-spermatogenic tissue of capybara testes, we analysed the relationship between testes mass and the size and ratio of the testes compartments and, indirectly, their activities. We found that the testes mass of the capybara is closely associated with the size of androgen-dependent scent glands and to the proportion of non-spermatogenic tissue in the testis. We further investigated the associations between variables related to dominance and to sexual characters. The results suggest that dominance in capybaras is more associated with androgen-dependent scent glands than with sperm production. We suggest that male capybaras compete for dominance with chemical and visual status signalling.     

Arrested development of secondary sexual adornments in subordinate adult male mandrills (Mandrillus sphinx).

Previous studies of semifree-ranging mandrills identified two morphological and social variants of the adult male, based on behavioral and secondary sexual characteristics. "Fatted" males are social, with highly developed sex skin coloration, large testes, high plasma testosterone levels, and fat rumps; while "nonfatted" males are peripheral or solitary, with paler sex skin, smaller testes, lower plasma testosterone, and slimmer rumps. We present a detailed study of morphology and group association for 10 adult male mandrills, living in two semifree-ranging groups in Gabon, in order to relate differences between males to dominance rank. The results show that rather than existing as two distinct morphotypes, male mandrills represent a continuous spectrum of possibilities between social males with fully developed secondary sexual characteristics, and solitary males with muted secondary sexual characteristics. Alpha males (N = 2) had the highest testosterone levels, the most colorful sex skin, and the most active sternal glands, and were the only males to spend 100% of their time with the social group. Rank relationships between nonalpha males (N = 8) were not always clear, but all subordinate males had lower testosterone levels and less development of the secondary sexual adornments, and were less group-associated than alpha males. These findings suggest that only alpha males have sufficient testosterone to develop full secondary sexual characteristics, and we propose possible socioendocrine mechanisms underlying the suppression of testosterone and secondary sexual development in subordinate adults. We discuss differences in secondary sexual development in relation to reproductive strategies, and discuss the evolution of alternative reproductive morphs in primates.