Non-gonadal mediated effect of photoperiod on hibernation and body weight cycles of the European hamster

1. Sexually active male European hamsters raised under short photoperiod display high levels of plasma testosterone, high body weight and do not hibernate. 2. Castrated males in May, raised under the same conditions, do not hibernate and do not present the physiological body weight rhythm. 3. Normal and castrated animals under natural conditions enter hibernation and display a normal body weight rhythm. 4. Normal and castrated animals not submitted to the natural succession of long and short days do not enter hibernation. 5. Photoperiod directly controls body weight and hibernation gonadal interactions.     

Influence of photoperiod and gonadal steroids on hibernation in the European hamster

Torpor was monitored daily in adult male and female European hamsters (Cricetus cricetus) induced to hibernate by exposure to a cold environment (6 degrees C). The effect of photoperiodic manipulations or administration of exogenous gonadal steroids was examined in gonadectomized or intact hamsters. 1. Gonadal regression occurred in all short day, but only in some long day, cold-exposed hamsters. Entry into hibernation was not observed until reproductive regression had occurred. Thus, gonadal atrophy appears to be a necessary precondition for hibernation. 2. Castrated hamsters in the short day cold condition showed a significantly greater incidence of torpor than those in the long day cold condition. Hence, photoperiod affected torpor independently of its effect on the gonadal cycle. 3. Testosterone, when administered via silastic capsules at near physiological levels, completely inhibited torpor in gonadectomized male and female hamsters hibernating in the short day cold condition. 4. In ovariectomized females, torpor was unaffected by progesterone treatment, but partially inhibited by estradiol. A greater inhibition of torpor was observed when estradiol-primed females were administered both estradiol and progesterone simultaneously. Thus, the effect of both hormones may be functionally comparable to that of the single testicular hormone. 5. Estradiol inhibited torpor to a greater extent in intact and ovariectomized female hamsters hibernating in long days than those in short days, suggesting an effect of photoperiod on responsiveness to estradiol. These results indicate an inverse relationship between the gonadal and hibernation cycles, and a probable role for gonadal steroids to influence the timing of the hibernation season. However, non-gonadal factors must also be involved in controlling hibernation, since photoperiod affected the incidence of torpor in gonadectomized animals and because hamsters were able to terminate hibernation in the absence of gonadal hormones.     

Photoperiodic influences on sexual behavior in male Syrian hamsters

The effect of photoperiodic conditions on sexual behavior was investigated in male Syrian hamsters that were either gonadally intact, or castrated and treated with low doses of testosterone throughout the experiment. Hamsters were exposed to long (LD 16:8) or short (LD 8:16) days for 7 weeks; for the next 8 weeks, either they were exposed to an intermediate daylength (LD 12:12), or daylength conditions remained unchanged. Sexual behavior was affected by photoperiod conditions in both gonadally intact animals and testosterone-treated castrates, but to different degrees. Intact males exposed to short days for 15 weeks exhibited gonadal regression, and their copulatory performance was impaired. The percentage of animals that intromitted or ejaculated was significantly reduced. Additional measures of sexual performance among the copulating males were also affected. In contrast, among the castrates with testosterone clamped at low but stable levels, the proportion of males that mounted, intromitted, or ejaculated was not affected by photoperiod. However, among the males that continued to copulate, sexual performance changes were present in the short-day castrates that resembled those displayed by the intact males. We infer that these behavioral effects in both hormonal conditions reflect primarily a difficulty in the attainment of intromission. Gonadal regression alone cannot easily account for the behavioral deficits of the intact males, because circulating testosterone levels at the end of the experiment were not significantly different between the gonadally intact hamsters and the castrated, testosterone-treated hamsters exposed continuously to short days. Males transferred from either long or short days to the intermediate-daylength condition responded behaviorally to this photoperiod as if it were a short day, that is, their ejaculatory frequency declined. We conclude that male hamsters exposed to photoinhibitory daylengths exhibit deficits in their sexual behavior, not only because endogenous levels of testosterone decrease, but also because the substrates on which this hormone acts become less responsive. We hypothesize that under physiological conditions, the episodic secretion of testosterone imposes constraints on the maintenance or restoration of copulation, and that the potent behavioral effects achieved by constant-release implants of testosterone may mask the presence of photoperiodically induced alterations in the hamster's sensitivity to this gonadal hormone.     

Influence of photoperiod and gonadal status on food intake, adiposity, and gene expression of hypothalamic appetite regulators in a seasonal mammal

We studied the effects of photoperiod on metabolic profiles, adiposity, and gene expression of hypothalamic appetite-regulating peptides in gonad-intact and castrated Soay rams. Groups of five to six animals were studied 6, 18, or 30 wk after switching from long photoperiod (LP: 16 h of light) to short photoperiod (SP: 8 h of light). Reproductive and metabolic indexes were measured in blood plasma. Expression of neuropeptide Y (NPY), proopiomelanocortin (POMC), and leptin receptor (ObRb) in the arcuate nucleus was measured using in situ hybridization. Testosterone levels of intact animals were low under LP, increased to a peak at 16 wk under SP, and then declined. Voluntary food intake (VFI) was high under LP in both intact and castrated animals, decreased to a nadir at 12-16 wk under SP, and then recovered, but only in intact rams as the reproductive axis became photorefractory to SP. NPY gene expression varied positively and POMC expression varied negatively with the cycle in VFI, with differences between intact and castrate rams in the refractory phase. ObRb expression decreased under SP, unrelated to changes in VFI. Visceral fat weight also varied between the intact and castrated animals across the cycle. We conclude that 1) photoperiodic changes in VFI reflect changes in NPY and POMC gene expression, 2) changes in ObRb gene expression are not necessarily determinants of changes in VFI, 3) gonadal status affects the pattern of VFI that changes with photoperiod, and 4) in the absence of gonadal factors, animals can eat less but gain adiposity.     

Energy metabolism, testosterone and corticosterone in white-crowned sparrows

The influence of the steroid hormones testosterone and corticosterone on energy metabolism and activity of birds is largely enigmatic. We measured resting metabolic rate during night and day in 12 long-term castrated and 12 intact male white-crowned sparrows (Zonotrichia leucophrys gambelii) under short-day (8:16 SD), long-day (20:4 LD), LD+testosterone implant and LD−testosterone implant conditions. Each male was sequentially measured under all four conditions. Photostimulation increased testosterone, resting metabolic rate, food intake, hopping activity and body mass in castrates and intact males. Surprisingly, testosterone levels and metabolic rates did not differ between intact and castrated males. Testosterone implantation increased activity and food intake, but decreased body mass and resting metabolic rate in both groups. Removing testosterone implants reversed the effects on resting metabolic rate, activity and food intake. Corticosterone levels, measured immediately at the end of metabolism measurements, showed birds were not stressed. Corticosterone had no apparent relationship with resting metabolic rate and there was no interaction between corticosterone and testosterone. Overall, positive changes in testosterone levels resulted in a decrease of resting metabolic rate. We speculate that testosterone increases activity, and birds compensate for increased activity metabolism by reducing resting metabolic rate. Accepted: 18 July 1999     

Hormonal changes and energy substrate availability during the hibernation cycle of Syrian hamsters

Animals have to adapt to seasonal variations in food resources and temperature. Hibernation is one of the most efficient means used by animals to cope with harsh winter conditions, wherein survival is achieved through a significant decrease in energy expenditure. The hibernation period is constituted by a succession of torpor bouts (hypometabolism and decrease in body temperature) and periodic arousals (eumetabolism and euthermia). Some species feed during these periodic arousals, and thus show different metabolic adaptations to fat-storing species that fast throughout the hibernation period. Our study aims to define these metabolic adaptations, including hormone (insulin, glucagon, leptin, adiponectin, GLP-1, GiP) and metabolite (glucose, free fatty acids, triglycerides, urea) profiles together with body composition adjustments. Syrian hamsters were exposed to varied photoperiod and temperature conditions mimicking different phases of the hibernation cycle: a long photoperiod at 20 °C (LP20 group), a short photoperiod at 20 °C (SP20 group), and a short photoperiod at 8 °C (SP8). SP8 animals were sampled either at the beginning of a torpor bout (Torpor group) or at the beginning of a periodic arousal (Arousal group). We show that fat store mobilization in hamsters during torpor bouts is associated with decreased circulating levels of glucagon, insulin, leptin, and an increase in adiponectin. Refeeding during periodic arousals results in a decreased free fatty acid plasma concentration and an increase in glycemia and plasma incretin concentrations. Reduced incretin and increased adiponectin levels are therefore in accordance with the changes in nutrient availability and feeding behavior observed during the hibernation cycle of Syrian hamsters.     

Modification of testicular and thyroid function by chronic exposure to short photoperiod: a comparison in four rodent species

Exposure of male Syrian hamsters (Mesocricetus auratus) for 10 weeks to short photoperiod (SP) providing 10 hr light: 14 hr darkness (10:14 LD) produced a significant reduction in the weights of the reproductive organs, plasma thyroxine (T4) levels and free T4 index (FT4I) compared to the values of animals exposed to long photoperiod (LP, 14:10 LD). C57bl male house mice (Mus musculus) kept in SP (10:14 LD) had reproductive organ weights equivalent to those of mice kept in long days (14:10 LD) and lower T3 uptake (T3U) values. Male gerbils (Meriones unguiculatus) exposed to 13 weeks of SP (10:14 LD) had lower body weights, testes and seminal vesicle weights and higher T3U values compared to LP (14:10 LD) controls. However, no effect was seen on plasma T4 and triiodothyronine (T3) values nor the FT4I and free T3 index (FT3I). White-footed male mice (Peromyscus leucopus) exposed to SP (8:16 LD) had significantly lower testes and seminal vesicle weights while plasma T4 and T3 levels were unaffected. Snell strain house mice (Mus musculus) exposed to SP (8:16 LD) had normal reproductive organ weights compared to the values of LP-exposed (16:8 LD) control animals. However, there was a significant depression in T3 and in the FT3I in the SP animals.     

Inhibition of hibernation by exercise is not affected by intergeniculate leaflets lesion in hamsters

The circadian clock of mammals, located in the suprachiasmatic nuclei (SCN) of the hypothalamus, has been demonstrated to integrate day length change from long (LP) to short photoperiod (SP). This photoperiodic change induces in Syrian hamsters a testicular regression through melatonin action, a phenomenon that is inhibited when hamsters have free access to a wheel. The intergeniculate leaflets (IGL), which modulate the integration of photoperiod by the SCN, are a key structure in the circadian system, conveying nonphotic information such as those induced by novelty-induced wheel running activity. We tested in hamsters transferred from LP to a cold SP the effects of wheel running activity on a photoperiod-dependent behavior, hibernation. Lesions of the IGL were done to test the role of this structure in the inhibition induced by exercise of photoperiod integration by the clock. We show that wheel running activity actually inhibits hibernation not only in sham-operated animals, but also in hamsters with a bilateral IGL lesion (IGLX). In contrast, IGL-X hamsters without a wheel integrate slower to the SP but hibernate earlier compared with sham-operated animals. Moreover, some hibernation characteristics are affected by IGL lesion. Throughout the experiment at 7 degrees C, IGL-X hamsters were in hypothermia during 18% of the experiment vs. 32% for sham-operated hamsters. Taken together, these data show that the IGL play a modulatory role in the integration of photoperiodic cues and modulate hibernation, but they are not implicated in the inhibition of hibernation induced by wheel running activity.     

Photoperiodic suppression of gonadotrophin secretion in castrated male hamsters

Male golden hamsters were transferred from long to short days and castrated on the day of transfer (Group SP0) or 1, 2 or 3 weeks afterwards (Groups SP1, SP2 & SP3). Animals in Group LP were castrated and maintained on long days. After 7 weeks of short days, plasma levels of LH and FSH were low in Groups SP1, SP2, and SP3. In Group SP0 LH output was also low and FSH secretion, although greater than in Groups SP1, SP2 and SP3, was lower than in the long-day controls (Group LP). This photoperiodic control of gonadotrophin secretion in castrated hamsters raises doubts about the significance of hypothetical alterations in hypothalamo-pituitary sensitivity to sex steroids.     

Effects of season on the secretion of LH and testosterone in intact and castrated red deer stags (Cervus elaphus).

At 2--4 monthly intervals during the year blood samples were collected every 15 min for 6 h from 2 intact and 3 castrated red deer stags to study the relationship between season and the secretion of LH and testosterone. In the intact stags plasma LH and testosterone concentrations changed during the year; the LH levels were maximal in August during the phase of testicular redevelopment, while the testosterone levels were maximal from September to November coinciding with the time of peak testicular activity and the mating season. The castrated stags had higher plasma levels of LH than the intact stags at all times of the year, and there was no clear seasonal cycle in LH levels in these animals.     

Sexual dimorphism in N-acetyltransferase activity, hydroxyindole-O-methyltransferase activity, and melatonin content in the Harderian gland of Syrian hamsters: changes following gonadectomy

The activities of N-acetyltransferase (NAT) and hydroxyindole-O-methyltransferase (HIOMT) and the melatonin content of the Harderian glands of intact and gonadectomized male and female Syrian hamsters were studied. NAT activity in intact male Harderian glands was twice that of the female. Prepubertal or adult castrated males exhibited a decrease in NAT activity to a level comparable to that seen in the female. Testosterone implants in the castrated males led to a recovery of the original male NAT levels. Intact male hamsters had very low levels of Harderian HIOMT activity and melatonin content in comparison with the glands of the females. Prepubertal gonadectomy but not castration of adult males raised the levels of HIOMT activity and the melatonin content to those of the females. Bilateral ovariectomy had no effect on melatonin content, NAT activity, or HIOMT activity in the female hamster Harderian gland.     

Effects of gonadal steroid hormones on hibernation in the Turkish hamster (Mesocricetus brandti)

Summary The Turkish hamster (Mesocricetus brandti) is a photoperiodic species in which exposure to a short day photoperiod induces gonadal atrophy. When hibernating male Turkish hamsters were administered testosterone via subcutaneous silastic capsules hibernation was abruptly terminated. The threshold serum testosterone level required to prevent hibernation was intermediate between the levels observed in males with fully-regressed and fully-functional testes. Dihydrotestosterone was as effective as testosterone in blocking hibernation. Estradiol had a partial inhibitory effect. Progesterone and corticosterone implants had no effect on hibernation. Similar results were obtained in female hamsters. The total period of hibernation for untreated males under laboratory conditions was usually 5–6 months. In most animals testicular growth began to occur toward the end of that period. As gonadal growth continued bouts of torpor decreased in frequency and duration, and hibernation was terminated when the testes approached reproductive size. Castrated males continued to hibernate much longer than intact animals. These observations suggest that in nature decreasing day length in the fall initiates gonadal regression which is followed by cold-induced hibernation. In the spring spontaneous recrudescence of the testes may lead to termination of the dormancy period. This mechanism may enable the species to prepare for the reproductive season with maximum efficiency.Supported by NIH Research Grant HD-10478 and by a grant from the Connecticut Research FoundationThe data in this paper were presented in part at the Annual Meeting of the American Society of Zoologists, Toronto, December 26–30, 1977     

Effects of photoperiod, melatonin implants and castration on molting and on plasma thyroxine, testosterone and prolactin levels in the European badger (Meles meles)

1. The seasonal molt, which lasts six months in the badger, begins in mid-July and ends at the beginning of winter. It occurs under natural long-day conditions, following the seasonal drop in plasma testosterone levels, concomitant with high levels of thyroxine and prolactin. 2. To examine the role of the different factors involved (day length, prolactin, thyroxine, testosterone), different groups of badgers, divided into subgroups of castrated or intact animals, were subjected to the influence of long days (20L: 4D), short days (4L:20D) or the effect of subcutaneous melatonin implants. 3. In all cases, castration resulted in a significantly earlier onset of molting 1-3 months, depending on the group, regardless of the experimental conditions (20L:4D, 4L:20D, melatonin). 4. However, molting started earliest in animals subjected to long days, irrespective of whether they were castrated or intact. 5. In the melatonin-implanted badgers, molting started either early (castrated animals), or late or not at all (intact animals). 6. Lastly, in castrated badgers subjected to experimental photoperiods (short days or long days) or melatonin implants, the period of molting was shortened from 6 months (intact outdoor animals) to 4 months. 7. The advance in shedding was always related to an early drop in testosterone (or an absence of testosterone in the castrated animals) and to a higher or earlier increase in thyroxine levels.(ABSTRACT TRUNCATED AT 250 WORDS)     

Effects of short days on aromatization and accumulation of nuclear estrogen receptors in the hamster brain

Exposure of hamsters to short days increases sensitivity to the negative feedback effects of testosterone (T) but decreases responsiveness to the behavioral effects of the hormone. Since T is metabolized in the brain to 5 alpha-dihydrotestosterone (DHT) and estradiol, which differentially affect gonadotropin secretion and sex behavior, it is reasonable to postulate that daylength can modulate neural responses by quantitative or qualitative alterations in T metabolism and subsequent receptor binding of active hormone. Experiments reported here focused on aromatization and the nuclear accumulation of estrogen receptors. Adult male hamsters were maintained for 6-12 wk in long (14:10 LD) or short (8:16 LD) daily photoperiods. Both intact and castrated animals were used to assess direct effects of short days versus changes due to short-day-induced testicular regression. Discretely dissected regions of the brain (preoptic area, POA; hypothalamus, HTH; and corticomedial amygdala, CMA) or limbic blocks (LIM) comprised of all three regions were assayed for estrogen-synthesizing activity (aromatase) and estrogen-binding activity (receptors). Aromatase was estimated in vitro by conversion of [7-(3)H] androstenedione to [3H] estrogen and in vivo by measuring increases in nuclear estrogen receptor levels after injection of aromatizable androgen. Receptor-binding activity was assayed in crude cytosolic and nuclear extracts by incubating samples with [3H] estradiol +/- 100-fold excess inert estradiol, and separating free and bound steroids by Sephadex LH-20 gel filtration. When aromatase was assayed in homogenates prepared from discrete brain regions of individual hamsters, significantly lower activity was found in the HTH of short-day animals than in long-day controls. This effect was seen in both intact and castrated animals, which indicates that it was not mediated by the testis. Decreased enzyme activity in the POA and CMA of short-day hamsters was not significant, nor was there an effect of castration independent of short days. Low levels of nuclear estrogen receptors were present in LIM of intact males, but these were reduced after castration or concomitant with testicular regression after short-day exposure. This suggests that the hamster testis normally secretes estrogen or aromatizable androgen. A single injection of estradiol or aromatizable androgen (T or androstenedione) increased nuclear receptors in LIM of castrated animals. Cytosolic receptors were not different in short-day vs. long-day hamsters, nor were there differences in nuclear receptor levels after a single estradiol injection.(ABSTRACT TRUNCATED AT 400 WORDS)     

Effects of castration and androgen replacement on male courtship behavior in the red-sided garter snake (Thamnophis sirtalis parietalis)

Following artificial hibernation, sexually mature male garter snakes (Thamnophis sirtalis parietalis) exhibited a decline in courtship behavior irrespective of castration, sham operation, or castration with testosterone replacement therapy. Behavior declined more rapidly in castrated animals with testosterone replacement than in castrated or sham-operated animals. In sham-operated animals, the decline in courtship was accompanied by changes in testicular weight and spermatogenic state from small spermatogenically inactive testes to large spermatogenically active testes. Serum androgen levels were more than fourfold greater in sham-operated animals than in castrated animals; cell height of the androgensensitive renal sex segment was greatest in castrated animals with testosterone replacement and least in castrated animals. These findings indicate that following artificial hibernation, male courtship behavior of T.s. parietalis is independent of the presence of the testes.     

Changes in the testicular binding of luteinizing hormone and plasma testosterone concentrations in the Djungarian hamster subjected to different photoperiods and temperatures and effects of long-term testosterone treatment on the binding

The effects of artificial photoperiod, temperature, and long-term testosterone treatment on testicular luteinizing hormone (LH) binding were studied in adult male Djungarian hamsters. In hamsters transferred to long-day (LD; 16 hr light, 8 hr dark) photoperiod 8 weeks after adaptation in short-day (SD; 8 hr light, 16 hr dark) photoperiod of 25 degrees C, testicular growth was associated with an increase in the total LH binding per two testes and a decrease in LH binding per unit testicular weight. Plasma testosterone levels reached a peak 47 days after transfer to LD and tended to decrease thereafter, while the testes continued growing. In contrast, when hamsters reared under LD conditions at 25 degrees C for 12 weeks were transferred to SD, testicular regression was associated with a decrease in plasma testosterone and the total LH binding per two testes and an increase in LH binding per unit testicular weight. A significant decrease in LH binding per unit weight compared to SD controls was observed in those hamsters exposed to SD with continuous testosterone treatment. The testosterone treatment tended to induce decrease in the total LH binding. Scatchard plot analyses of the binding suggested that changes in LH binding were due to changes in the number of binding sites. When sexually mature male hamsters were subjected for 8 weeks to two different ambient temperatures (7 degrees C and 25 degrees C) and photoperiods (LD and SD), the difference between the two temperature groups was statistically not significant regarding the weights of testes, epididymides, and prostates; plasma testosterone levels; and LH binding in either LD or SD group. These results suggest that photoperiod is a more important environmental factor than temperature for the regulation of testicular activity and LH receptors and that testosterone reduces the number of LH receptors per unit testicular weight in adult male Djungarian hamsters.     

Androgenic control of N-acetyltransferase activity in the harderian glands of the Syrian hamster is mediated by 5 alpha-dihydrotestosterone

N-acetyltransferase (NAT) activity in the Harderian glands of intact and gonadectomized male and female Syrian hamsters was evaluated. The exogenous administration of 5 alpha-dihydrotestosterone (DHT) to castrated males and intact females produced an increase in NAT values, which reached the values present in the glands of intact males. The administration of a 5 alpha-reductase inhibitor to intact males led to a decrease in NAT activity, suggesting that testosterone is converted in DHT within the glands. It is concluded that NAT activity in the Syrian hamster Harderian glands is under androgenic control, the active steroid being DHT.     

Testosterone increases N-acetyltransferase activity in both male and female Syrian hamster harderian glands

N-acetyltransferase (NAT) activity was studied in the Harderian glands of intact and castrated (with or without subcutaneous testosterone implants) male and female Syrian hamsters. Castration in male hamsters produced a significant drop in the NAT activity. Castrated males with testosterone implants had NAT activity levels comparable to those in intact males. Ovariectomy did not modify NAT activity. Ovariectomized hamsters with testosterone implants exhibited a significant increase in the Harderian NAT activity reaching the same values as those in the glands of the male hamsters.     

Melatonin-induced suppression of gonadotropin titers in male golden hamsters: Effect on gonadal feedback mechanisms

Daily subcutaneous injections of melatonin cause testicular regression and a decline in circulating gonadotropin levels in male hamsters maintained on long photoperiods. We examine here if a reduction in gonadotropin levels also occurs in castrates administered melatonin and if melatonin-regressed hamsters respond to castration with an increased release of pituitary gonadotropins — a typical “castration response.” Groups of intact and castrated male hamsters maintained on a photoperiod of LD 14:10 received subcutaneous injections of 15 ug melatonin/day. Controls received vehicle only. After 7 weeks of injections the intact males were castrated. All animals were sacrificed a few days later and serum was assayed for gonadotropin titers. Melatonin injections caused a marked decline in serum gonadotropins in castrates and in intact males also caused testicular regression. In the latter, no “castration response” was observed upon removal of the testes. Thus, daily injections of melatonin depress serum gonadotropins in castrate and intact males and block the castration-associated rise in circulating gonadotropins in the latter.     

Sex-influenced population kinetics of Leishmania donovani in hamsters

Susceptibility of animals to infections depends upon various factors including sex of the host which plays a pivotal role. The intake of L. donovani was investigated in male and female hamsters as also in gonadectomized and hormone (sex) treated animals. Male hamsters developed more parasites (55/100 cell nuclei) than their female counterparts (22/100 cell nuclei). The hamsters receiving testosterone (250 micrograms/animal for 7 days) exogenously (im) had enhanced parasitic count (1.1-fold in male and 1.5-fold in females with respect to their respective controls). Administration of estradiol (3 micrograms/animal for 3 days) suppressed the infection in males by 2.5-fold and in female by 1.94-fold. Castration lowered the parasite 'in take' while ovarectomy promoted infection. In these (gonadectomized) animals the administration of testosterone in males restored parasite load while the estradiol therapy in females suppressed the infection. The results suggest a definite modulatory role of sex hormone, in the susceptibility of hamsters to L. donovani infection.