Neuroanatomical Distribution and Variations across the Reproductive Cycle of Aromatase Activity and Aromatase-Immunoreactive Cells in the Pied Flycatcher (Ficedula hypoleuca)

The anatomical distribution and seasonal variations in aromatase activity and in the number of aromatase-immunoreactive cells were studied in the brain of free-living male pied flycatchers (Ficedula hypoleuca). A high aromatase activity was detected in the telencephalon and diencephalon but low to negligible levels were present in the optic lobes, cerebellum, and brain stem. In the diencephalon, most aromatase-immunoreactive cells were confined to three nuclei implicated in the control of reproductive behaviors: the medial preoptic nucleus, the nucleus of the stria terminalis, and the ventromedial nucleus of the hypothalamus. In the telencephalon, the immunopositive cells were clustered in the medial part of the neostriatum and in the hippocampus as previously described in another songbird species, the zebra finch. No immunoreactive cells could be observed in the song control nuclei. A marked drop in aromatase activity was detected in the anterior and posterior diencephalon in the early summer when the behavior of the birds had switched from defending a territory to helping the female in feeding the nestlings. This enzymatic change is presumably controlled by the drop in plasma testosterone levels observed at that stage of the reproductive cycle. No change in enzyme activity, however, was seen at that time in other brain areas. The number of aromatase-immunoreactive cells also decreased at that time in the caudal part of the medial preoptic nucleus but not in the ventromedial nucleus of the hypothalamus (an increase was even observed), suggesting that differential mechanisms control the enzyme concentration and enzyme activity in the hypothalamus. Taken together, these data suggest that changes in diencephalic aromatase activity contribute to the control of seasonal variations in reproductive behavior of male pied flycatchers but the role of the telencephalic aromatase in the control of behavior remains unclear at present.     

Influence of environmental events immediately after birth on postnatal testosterone secretion and adult sexual behavior in the male rat

A rise in plasma testosterone (T) levels occurs in male rats during the first 2 hr after birth which is of importance for the process of sexual differentiation. To study the influence of environmental factors on the postnatal T surge and sexual development, newborn male rats were subjected to various treatments immediately after cesarean delivery including cooling, ether anesthesia, and mother-infant separation. In adulthood, the animals were observed for masculine and feminine sexual behavior. Males anesthetized at 0 hr showed elevated levels of feminine sexual behavior and impaired masculine sexual behavior. Pups subjected to cooling or mother-infant separation showed slightly prolonged intromission latencies, but otherwise normal levels of feminine sexual behavior. Significantly elevated plasma T levels were found in intact pups 2 hr after birth but not in pups subjected to cooling or ether anesthesia. Significantly higher levels of T were observed in pups subjected to cooling 4 hr after birth, suggesting a delay of the T surge. The most pronounced impairing effects were seen in the defeminization process, but the masculinization process also is affected by ether anesthesia. It was concluded that ether anesthesia immediately after birth may permanently interfere with the sexual development by suppressing the neonatal T surge.     

Territorial aggression, circulating levels of testosterone, and brain aromatase activity in free-living pied flycatchers

Testosterone (T) is a critical endocrine factor for the activation of many aspects of reproductive behavior in vertebrates. Castration completely eliminates the display of aggressive and sexual behaviors that are restored to intact level by a treatment with exogenous T. There is usually a tight correlation between the temporal changes in plasma T and the frequency of reproductive behaviors during the annual cycle. In contrast, individual levels of behavioral activity are often not related to plasma T concentration at the peak of the reproductive season suggesting that T is available in quantities larger than necessary to activate behavior and that other factors limit the expression of behavior. There is some indication from work in rodents that individual levels of brain aromatase activity (AA) may be a key factor that limits the expression of aggressive behavior, and in agreement with this idea, many studies indicate that estrogens produced in the brain by the aromatization of T may contribute to the activation of reproductive behavior, including aggression. We investigated here in pied flycatcher (Ficedula hypoleuca) the relationships among territorial aggression, plasma T, and brain AA at the peak of the reproductive season. In a first experiment, blood samples were collected from unpaired males holding a primary territory and, 1 or 2 days later, their aggressive behavior was quantified during standardized simulated territorial intrusions. No relationship was found between individual differences in aggressive behavior and plasma T or dihydrotestosterone levels but a significant negative correlation was observed between number of attacks and plasma corticosterone. In a second experiment, aggressive behavior was measured during a simulated territorial intrusion in 22 unpaired males holding primary territories. They were then immediately captured and AA was measured in their anterior and posterior diencephalon and in the entire telencephalon. Five males that had attracted a female (who had started egg-laying) were also studied. The paired males were less aggressive and correlatively had a lower AA in the anterior diencephalon but not in the posterior diencephalon and telencephalon than the 22 birds holding a territory before arrival of a female. In these 22 birds, a significant correlation was observed between number of attacks/min displayed during the simulated territorial intrusion and AA in the anterior diencephalon but no correlation was found between these variables in the two other brain areas. Taken together, these data indicate that the level of aggression displayed by males defending their primary territory may be limited by the activity of the preoptic aromatase, but plasma T is not playing an important role in establishing individual differences in aggression. Alternatively, it is also possible that brain AA is rapidly affected by agonistic interactions and additional work should be carried out to determine whether the correlation observed between brain AA and aggressive behavior is the result of an effect of the enzyme on behavior or vice versa. In any case, the present data show that preoptic AA can change quite rapidly during the reproductive cycle (within a few days after arrival of the female) indicating that this enzymatic activity is able to regulate rapid behavioral transitions during the reproductive cycle in this species.     

Effects of long-acting testosterone administration on testes in free living pied flycatchers Ficedula hypoleuca

Male pied flycatchers Ficedula hypoleuca given injections of long-acting testosterone, when in full breeding condition, maintained spermatogenesis. In males given vehicle only and in untreated males the testes collapsed at the time of hatching of the brood. The number and secretory activity of the Leydig cells, as indicated by enzymic activities, were markedly lowered after testosterone administration. The results make it unlikely that testosterone is responsible for testicular regression in this species, but it may affect the mechanism regulating the number and activity of the Leydig cells.     

Testosterone, ticks and travels: a test of the immunocompetence-handicap hypothesis in free-ranging male sand lizards.

The immunocompetence-handicap hypothesis suggests that androgen-dependent male characters constitute honest signals of mate and/or rival quality because of the imposed costs through immune suppression associated with elevated testosterone levels. We demonstrate in a field experiment that male sand lizards (Lacerta agilis) exposed to elevated testosterone suffered from increased mass loss and tick load compared to control males. Although the first of these two results could be due to an elevated basal metabolic rate from increased plasma testosterone levels, the increased parasite load was statistically independent of the loss in body condition and is likely to be due to compromised immune function. Testosterone-treated males showed greater mobility than control males, and greater mobility resulted in higher mating success. Our experiment thus lends support to the immunocompetence-handicap hypothesis, suggesting that male testosterone levels have been moderated by balancing selection for reproductive success and sustained immune function.     

Variation of lymphoid activity in the spleen of a migratory bird,the pied flycatcher (Ficedula hypoleuca; Aves,passeriformes)

The size and microscopic structure of the spleen of the migratory pied flycatcher (Ficedula hypoleuca) show marked changes during the reproductive cycle. Upon the spring return to their northern breeding sites, the birds have a small spleen with little lymphoid activity and a poorly developed red pulp. During the breeding period the volume of red and white pulp increases, the number and distinctness of lymphoid follicles (germinal centres) in the white pulp increase, and groups of cells with intensely basophilic cytoplasm, probably B cells (plasma cells), appear. The findings suggest that the immune system of the adult pied flycatcher is activated during periods when it is bound to the nest. Young flycatchers beginning their autumn migration also show a marked increase of lymphoid activity in the spleen.     

The abnormal conduct of capercaillies Tetrao urogallus.

The frequency, behavior, and testosterone levels of deviant capercaillies were studied in southern Finland. Roughly 1% of the population was estimated to behave abnormally. Deviant males display and show threatening behavior toward not only humans, but also attacked stuffed capercaillie males and without hesitation copulated with a stuffed female. Deviant females appear tame and crouch in front of humans, but avoid males. The testosterone level in deviant males was about five times higher than that of normal displaying males. The origin of this striking phenomenon is still unclear, although it must be connected with display. Two, though not mutually exclusive, proximate mechanisms for the development of this abnormal behavior are presented: anomalous sex hormone concentrations and incorrect sexual imprinting. The ultimate reason for the apparent increase in numbers of deviant capercaillies is probably logging which diminishes populations and, thereby, favors the spreading of abnormal behavior.     

Effects of corticosterone on territorial behavior of free-living male song sparrows Melospiza melodia

A group of 10 territorial male song sparrows, Melospiza melodia, were given subcutaneous implants of corticosterone in Silastic tubing. A second group of 10 territorial males were given empty implants as controls. After 18-24 hr all males were then subjected to a simulated territorial intrusion (STI) by placing a caged male song sparrow in the center of the subject's territory, and playing tape recorded songs through a speaker placed alongside. Significantly fewer males with corticosterone implants responded to STI than to controls, and the latency to respond was longer. Of the 3 experimental males that did respond to STI, all had a lower frequency of songs and did not approach the simulated intruder as closely as controls. Many males were captured 2-7 days after implantation and blood samples collected for measurement of circulating hormone levels. As expected, plasma levels of corticosterone were high in the group given corticosterone implants. However, plasma levels of luteinizing hormone (LH) were not affected by treatment with corticosterone, and although circulating levels of testosterone were depressed slightly compared with controls, they were within the normal range for territorial and breeding males. There were no differences in body mass despite greatly increased fat depots in males treated with corticosterone. These data suggest that high levels of corticosterone, similar to those measured during stressful episodes both in the laboratory and field, may suppress territorial behavior independently of the adenohypophysial-gonad axis. Since plasma levels of LH and testosterone are not depressed markedly, thus maintaining the gonads in a near functional state, renesting can begin as soon as environmental conditions ameliorate. Such mechanisms could potentially increase the probability of raising viable young after unpredictable, severe weather resulted in failure of the previous breeding attempt.     

Hormonal correlates of male attractiveness during mate selection in the mallard duck (Anas platyrhynchos)

The aims of the present study were (1) to examine if feeding condition prior to mating influences male hormone levels and behavior, (2) to evaluate the effect of age on male hormone levels, (3) to examine a possible association between male social display activity and four steroid hormones (testosterone, dihydrotestosterone, estrogen, and corticosterone), and (4) to examine if female behavior influences male hormone levels. Thirty male and fifteen female mallards were used in this study. Observations were made on a mixed flock of mallards for 10 consecutive days in autumn. Five weeks before the observations, males were randomly assigned to a feeding regime with either an unlimited food supply (UL group) or a limited food supply (L group). Males in the UL group showed significantly greater social display activity compared to the L group males. Females never incited (courted) males from the L group. Dihydrotestosterone levels were significantly higher in males showing social display activity as compared to males not showing these behavior patterns. Testosterone levels were significantly higher in males incited by females compared to males not incited by females.     

Enzyme histochemical studies in testes and seminal vesicles of the Pied flycatcher (Ficedula hypoleuca) during the breeding season

Enzymatic conditions in testes and seminal vesicles of the Pied flycatcher during the breeding season were studied by histochemical techniques. The following enzyme activities were studied: glucose-6-phosphatase dehydrogenase (G-6-PDH), NADPH₂-diaphorase, glutamic dehydrogenase (GDH), NADH₂-diaphorase, adenosine triphosphatase (ATPase) and acid phosphatase. Phospholipids and PAS-positive substances were also studied. Towards the end of the nest-building period, a time when the males showed maximal sexual activities, some enzyme activity changes were observed. There was an increase of the GDH activity in the sperm bundles, an increase of the ATPase activity in the interstitium and tunica propria of the tubuli seminiferi. The phospholipid content increased in all spermatogenetic cells and the PAS-positive material increased in the Sertoli cells and spermatozoa. The enzymic activities indicated a steroid production in the Leydig cells.
The epithelium of the seminal vesicles did not show any variations in enzyme activities as long as the Leydig cells persisted. Most enzymes showed a very high activity during this time, indicating a secretory function of the epithelium. The amount of phospholipids increased at the end of the nest-building period. Parallel with the degeneration of the epithelium the enzymic activities, as well as the phospholipid content, were lowered markedly.