The effects of androgen and antiandrogen on dominance and aggressiveness in male red-winged blackbirds

Male red-winged blackbirds were given implants of testosterone or flutamide in order to manipulate the level of androgen reaching receptor sites. Implants of cholesterol were given as controls. Radioimmunoassay showed higher levels of testosterone and DHT in the plasma of testosterone-implanted birds than in the plasma of the pooled flutamide-implanted and cholesterol-implanted birds. Dominance was significantly correlated with effective androgen level. Androgen level was not correlated with rates of supplantations per subordinate but was correlated with rates of escalated attacks per subordinate. Thus androgen level influences dominance in male red-winged blackbirds by influencing one component of aggressiveness.     

Social correlates of testosterone and ornamentation in male mandrills

We investigated relationships between fecal androgen concentrations, facial coloration and behaviour in semi-free-ranging male mandrills. We found that fecal androgen levels were significantly positively related to dominance rank, independent of rank stability and the mating period, suggesting that male mandrills live in a permanently aggressive context in which they must actively maintain their dominance status. Facial red coloration was also significantly related to both fecal androgen levels and rank, with high ranking males having both higher androgen levels and redder faces, although dominant males did not always have the highest androgen levels or the reddest faces. Predictive relationships between androgen levels, coloration and rank were short-term. Androgen concentrations and facial redness both increased in the presence of receptive females, as did the former during periods of rank instability. We conclude that male facial redness is likely to represent an honest signal (to other males) of current androgen status, competitive ability and willingness to engage in fights and that females may also use this to assess male condition. Further, our findings provide support for the “challenge hypothesis” as originally proposed for birds by Wingfield.     

Hormonal Responses of Male Gerbils to Stimuli from Their Mate and Pups

Following copulation and cohabitation with a pregnant female, male gerbils show high levels of parental behavior toward their pups. The initiation of male parental behavior may be the result of neuroendocrine changes induced by cohabiting with the pregnant female or by pup stimuli. Experiment 1 examines the changes in androgen and prolactin levels in male gerbils cohabiting with females over the reproductive cycle. Gerbils were mated and blood samples taken from males for hormone analysis 1, 10, and 20 days after pairing and 3, 10, and 20 days after pups were born. A group of unmated male gerbils served as controls. Plasma prolactin levels of males were elevated throughout the female's pregnancy and lactation periods, but were only statistically significantly higher than those of unmated males 20 days after pups were born. Androgen levels rose during pregnancy and dropped significantly after the birth of the pups. These hormonal changes are similar to those found in males of monogamous birds and differ from those found in males of polygynous rodents such as the rat. Experiment 2 examined the hormonal responses of male and female gerbils to pup replacement after 4 hr of parent–pup separation. Female gerbils showed a significant elevation of prolactin levels 1 hr after pup replacement, but males did not. Males with pups returned showed no difference in androgen levels from males who did not have pups returned. Thus, male gerbils show neuroendocrine changes following long-term cohabitation with their mate and pups, but do not show acute hormone responses to pup removal and replacement. These results indicate that parental males have neuroendocrine changes associated with parental behavior and these differ from the neuroendocrine changes underlying female parental behavior.     

Testosterone, testis size, seasonality, and behavior in group-living stumptail macaques (Macaca arctoides)

During a 28-month period, data were collected on physiological parameters and sociosexual behavior of 13 adult male members of a large mixed-sex group of stumptail macaques living in an outdoor cage. Monthly measurements of plasma testosterone, testis size, and body weight revealed no systematic seasonality. Seasonal variations did occur in branch shaking and grooming (both with low rates in winter), but not in other behaviors studied (copulation, masturbation, aggression). Dominance ranks were stable throughout the study period and were not significantly correlated with mean testosterone levels. Temporal fluctuations in behavioral frequencies did not parallel testosterone fluctuations. Interindividual differences in behavioral frequencies were often correlated with dominance rank, but not with testosterone levels.     

Changes in body mass and hormone levels between wintering and spring staging areas in dark-bellied brent geese Branta bernicla bernicla

We document seasonal changes in body mass and plasma hormone levels (testosterone and triiodothyronine) between winter and spring quarters in dark-bellied brent geese Branta bernicla bernicla. Body mass increased between winter and spring, whereas body size was the same for the birds sampled in winter and those in spring. Adults and males were larger and heavier than juveniles and females. Plasma testosterone levels did not differ significantly between winter and spring, and did not vary with sex, age and morphometry. Plasma triiodothyronine (T₃) levels were significantly higher in spring than in winter, and were higher for males than for females. However, T₃ levels did not vary significantly with age and body measurements. To explain the findings, we discuss potential impacts of social dominance.     

Does testosterone determine dominance in the house sparrow Passer domesticus? An experimental test

Badges of status function in many birds within a social context to establish dominance hierarchies and reduce antagonistic encounters. In order to maintain the honesty of the signalling system, such badges must be costly to produce or to maintain. The chest bib of the house sparrow functions as a badge of status and changes in size are known to be controlled by testosterone levels. We sought to test the relative importance of testosterone as opposed to bib size in determining dominance within a group of male house sparrows. We did this by manipulating testosterone levels independently during both breeding and post‐breeding seasons in experimental birds and examining the effect of testosterone titre, as well as corticosterone titre relative to bib size on dominance levels. Dominance hierarchies within the groups were tested during both the breeding and post‐breeding phases. We compared the results of these tests with dominance among intact (unmanipulated) birds. Results suggested that the breeding season dominance levels were largely determined by testosterone levels as well as bib size, whereas the post‐breeding dominance levels were determined by post‐breeding testosterone titre and previous breeding season dominance level. Within unmanipulated birds, basal corticosterone levels were significantly, negatively correlated with dominance level, but only during the breeding season. The influence of breeding season dominance on post‐breeding dominance suggests social history is important in determining dominance interactions as well as current testosterone levels and bib size.     

Environmental regulation of the reproductive system in a flexibly breeding Sonoran Desert bird, the Rufous-winged Sparrow, Aimophila carpalis

We investigated reproductive regulation in male Rufous-winged Sparrows, Aimophila carpalis, a Sonoran Desert passerine that breeds after irregular summer rains. Field and captive data demonstrate that increased photoperiod stimulates testicular development in March and maintains it until early September. Free-living birds caught in July and placed on captive long days (16L: 8D) maintained developed testes for up to 7 months, and free-living birds caught in September, during testicular regression, redeveloped testes when placed on captive long days, indicating that these birds were still photosensitive. Captive birds on long days maintained testicular development when exposed to temperatures mimicking those occurring during regression in free-living birds. In free-living birds, testicular development was observed during spring and summer, but unless this was associated with rainfall, breeding (indicated by juveniles) did not occur. Large increases in plasma luteinizing hormone (LH) in free-living males were correlated with heavy rainfall in July/August, when the birds bred, and in November, when they did not breed. In captive birds, plasma LH concentrations were unresponsive to photoperiodic changes, but may have responded to social cues. Plasma prolactin concentrations were directly correlated with photoperiod in free-living birds, but an effect of photoperiod on prolactin secretion was not seen in captive birds. It is concluded that male Rufous-winged Sparrows use long photoperiods to stimulate and maintain testicular development, but exposure to long photoperiods does not terminate breeding by inducing absolute photorefractoriness. The specific timing of reproductive behaviors is apparently determined by elevated plasma LH coinciding with long day stimulated gonad development.     

Androgens and male mating behavior in rough-skinned newts, Taricha granulosa

Cyproterone acetate was administered either orally or intraperitoneally to intact, adult male newts, Taricha granulosa. The number of males that exhibited the courtship behavior of clasping when tested with nuptial females was not altered by the antiandrogen treatments. In males which were unresponsive to nuptial females, the occurrence of clasping was not evoked by injections for 4 days of testosterone, dihydrotestosterone, or 11-ketotestosterone. Further, the incidence of clasping was not significantly elevated by injections of prolactin and/or testosterone for 30 days. The effect of sexual activity on testosterone and dihydrotestosterone levels in male newts was determined by radioimmunoassay of plasma collected from males which were: (1) isolated from females; (2) allowed to clasp a female for 2 min; or (3) allowed to clasp a female for 1 hr. The testosterone and dihydrotestosterone levels were unchanged during this period of clasping. In February and again in June, plasma androgen concentrations were measured in males which differed in their propensity to initiate courtship when paired with females. Androgen levels were similar for males that clasped a female and males that never attempted to clasp a female. Plasma androgen levels in the male newt are apparently not correlated with sexual responsiveness.     

Endocrine correlates of rank,reproduction, and female-directed aggression in male Japanese macaques (Macaca fuscata)

Fecal testosterone and cortisol levels in six wild male Japanese macaques (Macaca fuscata), three of high rank and three of low, were analyzed to investigate the hormonal correlates of rank, reproduction, and female-directed aggression. The study encompassed the 6-month mating season, from October 1999 to March 2000, during which time 251 fecal samples and approximately 550 h of behavioral data were collected. Dominant males were not found to differ from subordinate males in overall rates of aggressive or copulatory behavior. Likewise, testosterone excretion, which peaked in the early part of the mating season and declined gradually thereafter, did not differ significantly by rank. High-ranking males, however, were observed to excrete significantly higher levels of cortisol than low-ranking males, suggesting that dominance may carry costs. The two hormones were found to be inversely correlated in the two most dominant males, but independent in all others. Rate of noncontact aggression was significantly correlated with testosterone, while no significant relationships were observed between testosterone and contact aggression nor any aspect of copulatory behavior. These data further support the contention that social subordinance and stress are not inexorably linked, as well as suggest that elevated glucocorticoid concentrations in high-ranking males may reflect increased metabolic costs associated with dominant male reproductive strategy.     

Corticosterone treatment has no effect on reproductive hormones or aggressive behavior in free-living male tree sparrows, Spizella arborea

We examined the effect of corticosterone on plasma levels of reproductive hormones (testosterone, dihydrotestosterone, and luteinizing hormone) and territorial defense behavior in male tree sparrows, Spizella arborea. Birds receiving Silastic implants filled with corticosterone (B) had significantly higher plasma levels of B than control birds, which received empty implants, and exhibited pectoral muscle wastage and a decrease in body mass. We evaluated the hormonal and agonistic responses of the two implanted groups of birds using a simulated territorial intrusion (STI) 2 to 4 days after they were implanted. Corticosterone-treated and control birds did not differ in their circulating levels of reproductive hormones or in their behavioral responses to STI (latency to respond to intrusion, number of songs, and closest approach to a decoy and tape recording). Unlike previous studies of north temperate passerines, high physiological levels of exogenous B had no effect either on circulating levels of reproductive hormones or on territorial behaviors associated with breeding. Nonetheless, untreated tree sparrows do mount a robust adrenocortical response, having a two- to fourfold increase in plasma B levels during a 1-h period of capture. Thus, adrenocortical responsiveness is maintained in these birds, but elevated levels of glucocorticoids do not suppress reproductive hormones or associated behaviors. We believe that this hormonal and behavioral refractoriness to glucocorticoids-or uncoupling of the stress response from the reproductive axis-may be advantageous for species having extreme temporal constraints on their breeding schedules.     

The natural plasma testosterone profile of male blue tits during the breeding season and its relation to song output

In male birds, the gonadal hormone testosterone (T) is known to influence territorial and mating behaviour. Plasma levels of T show seasonal fluctuations which vary in relation to mating system and social instability. First, we determined the natural T profile of male blue tits Parus caeruleus during the breeding season. We found that plasma levels of T increased at the onset of nest building. Thus, the increase in circulating T was not associated with territory establishment, nor with the fertile period of the males' mates. In most individuals, T levels dropped to values close to zero during the period of chick feeding. Second, we investigated the relationship between plasma levels of T and male age, size, and singing behaviour. During the mating period, T levels did not differ between 1 yr old and older males and did not correlate with body size or condition. However, song output during the dawn chorus tended to be positively correlated with T levels. Therefore, if high T levels are costly, song output might be an honest indicator of male quality in blue tits. Finally, we show that plasma levels of T are significantly higher during the night than during the day. This pattern has also been observed in captive non-passerine birds, but its functional significance remains unknown.     

Relationships between hormones and aggressive behavior in green anole lizards: an analysis using structural equation modeling

We investigated the relationship between aggressive behavior and circulating androgens in the context of agonistic social interaction and examined the effect of this interaction on the androgen-aggression relationship in response to a subsequent social challenge in male Anolis carolinensis lizards. Individuals comprising an aggressive encounter group were exposed to an aggressive conspecific male for 10 min per day during a 5-day encounter period, while controls were exposed to a neutral stimulus for the same period. On the sixth day, their responses to an intruder test were observed. At intervals, individuals were sacrificed to monitor plasma androgen levels. Structural equation modeling (SEM) was used to test three a priori interaction models of the relationship between social stimulus, aggressive behavior, and androgen. Model 1 posits that exposure to a social stimulus influences androgen and aggressive behavior independently. In Model 2, a social stimulus triggers aggressive behavior, which in turn increases circulating levels of androgen. In Model 3, exposure to a social stimulus influences circulating androgen levels, which in turn triggers aggressive behavior. During the 5 days of the encounter period, circulating testosterone (T) levels of the aggressive encounter group followed the same pattern as their aggressive behavioral responses, while the control group did not show significant changes in their aggressive behavior or T level. Our SEM results supported Model 2. A means analysis showed that during the intruder test, animals with 5 days of aggressive encounters showed more aggressive responses than did control animals, while their circulating androgen levels did not differ. This further supports Model 2, suggesting that an animal's own aggressive behavior may trigger increases in levels of plasma androgen.     

Correlation of simultaneously determined plasma insulin and glucose levels in fasting and mildly or severely stressed raptors

Plasma insulin and glucose levels were simultaneously determined in 60 fasting raptors (seven species) which had experienced mild or severe stress: prolonged confinement in flight cages (Type A), and serious debilities such as fractured bones, soft-tissue damage and/or starvation (Type B) respectively. Two of the species contained Types A and B (43 birds) while the remaining five species (17 birds) were of Type B only. Wide ranges in plasma insulin (0-135 pg/ml or 0-3.0 microU/ml) were observed in both Types A and B. Mean levels were not significantly different between species, although levels in Type B tended to be lower than those in Type A. Wide ranges in plasma glucose (195-485 mg/dl) were also observed in Types A and B but mean levels between species were remarkably similar, and likewise were not significantly different. However, even though mean insulin and glucose levels did not differ significantly between mildly or severely stressed and fasting birds, a low-level but significant (P less than 0.001) correlation (r = 0.5772) between insulin and glucose levels existed. This suggests that insulin contributes minimally, but significantly, to regulation of plasma glucose levels during stressful experiences or the fasting state.     

Spatial ability is impaired and hippocampal mineralocorticoid receptor mRNA expression reduced in zebra finches (Taeniopygia guttata) selected for acute high corticosterone response to stress

In mammals, stress hormones have profound influences on spatial learning and memory. Here, we investigated whether glucocorticoids influence cognitive abilities in birds by testing a line of zebra finches selectively bred to respond to an acute stressor with high plasma corticosterone (CORT) levels. Cognitive performance was assessed by spatial and visual one-trial associative memory tasks. Task performance in the high CORT birds was compared with that of the random-bred birds from a control breeding line. The birds selected for high CORT in response to an acute stressor performed less well than the controls in the spatial task, but there were no significant differences between the lines in performance during the visual task. The birds from the two lines did not differ in their plasma CORT levels immediately after the performance of the memory tasks; nevertheless, there were significant differences in peak plasma CORT between the lines. The high CORT birds also had significantly lower mineralocorticoid receptor mRNA expression in the hippocampus than the control birds. There was no measurable difference between the lines in glucocorticoid receptor mRNA density in either the hippocampus or the paraventricular nucleus. Together, these findings provide evidence to suggest that stress hormones have important regulatory roles in avian spatial cognition.     

Control of aggression and dominance in white-throated sparrows by testosterone and its metabolites

In three experiments, we investigated whether testosterone itself or its metabolites activate aggression and dominance in white-throated sparrows Zonotrichia albicollis. Groups of five to six sparrows, each treated with a different steroid implanted subcutaneously, were observed in outdoor aviaries during late winter to determine the birds' rates of aggression (supplantations and attacks scaled to the number of available subordinates) and dominance rankings with opponents not previously encountered. In Experiment 1, testosterone (T) had a greater effect on aggression and dominance than did androstenedione, 5α-dihydrotestosterone (D), androsterone, or estradiol (E). In Experiment 2, birds with T or D + E had higher aggression scores and dominance ranks than birds with either D or E alone. Birds with T and D + E did not differ. The testosterone metabolites, D and E, thus acted synergistically to determine rates of aggression and dominance ranks. To corroborate these results, in Experiment 3 we treated T-implanted birds with the following blocking agents: ATD, expected to reduce conversion of T to E (AT birds); progesterone, expected to reduce conversion of T to D (PT birds); or both (APT birds). The APT birds had lower aggression scores and dominance ranks than did AT or PT birds, despite having higher mean levels of circulating T than AT or PT birds or birds implanted with T alone. Cyproterone acetate also reduced aggression scores and dominance in T-implanted birds. We conclude that the hormonal control of aggression and dominance in these birds requires conversion of testosterone to both androgenic and estrogenic metabolites.     

The hormonal regulation of premigratory fat deposition and winter fattening in red-winged blackbirds

Glucagon is a highly potent lipolytic agent in birds and a candidate for regulating premigratory and winter fattening. The seasonal role of glucagon in fat metabolism was determined by monitoring plasma glucagon, fatty acids and glucose in two groups of red-winged blackbirds; one group exposed to outside environmental conditions (September to May) and a second group maintained at summer conditions with respect to day length and temperature. The results of this investigation demonstrate significantly lower plasma glucagon (480.1 pg/ml) in birds exposed to outdoor conditions than in birds maintained at summer conditions (734.6 pg/ml) during September/October. The data are consistent with the view that low plasma glucagon in outdoor birds ensures the preservation of fat stores for autumn migration. Lower plasma free fatty acid (FFA) levels (0.35 mEq/l) in outdoor birds (vs. 0.54 mEq/l in indoor birds) in autumn may reflect the rapid transport of FFA to adipose tissue for lipogenesis resulting in a steady increase in body weight from September to January. The sharp decline in plasma FFA in indoor birds from 0.54 mEq/l in September/October to 0.28 mEq/l in January/February may be attributed to a marked decrease in food consumption, rather than a dramatic change in the rate of lipid transport from blood to muscle or adipose tissue. Glucagon injections caused a 600% increase in plasma FFA and a more modest (50%) increase in plasma glucose. This confirms the major role of glucagon in fat mobilization. Its lipolytic effects, however, can vary seasonally by way of down regulation of glucagon receptors. Down regulation of glucagon receptors in adipose tissue and the associated reduced sensitivity of adipocytes to the lipolytic action of glucagon would account for the progressive increase in weight of the birds throughout November/December when plasma glucagon levels were significantly higher (578.9 pg/ml) in outdoor birds as compared to indoor birds (436.9 pg/ml). Lower plasma glucagon levels (405.5 pg/ml) in outdoor birds in January/February (vs. 638.6 pg/ml in indoor birds) may reflect the same physiological conditions prevailing in September/October favoring the preservation of fat stores.     

Androgen and the elaborate courtship behavior of a tropical lekking bird

In most bird species, male courtship behavior is controlled by testosterone (T) and its metabolites. In species breeding in temperate and arctic regions T circulates at high levels during a relatively short courtship period because high levels of T can be costly in terms of immunocompetence and parental care. Few studies have investigated androgen modulation of courtship behavior in tropical birds. Male golden-collared manakins (Manacus vitellinus) aggregate in leks for several months and perform spectacular, acrobatic courtship displays. Here we examined whether T is elevated in golden-collared manakins during the displaying period and if courtship behavior is modulated by androgen action on androgen receptors. We measured T levels in displaying males at the beginning of the breeding season and again, one month later. In addition, both wild and captive males were treated with the anti-androgen, flutamide, and their courtship behavior was recorded for several weeks. T levels were relatively high shortly after leks were established but decreased substantially a month later, even though the amount of courtship did not change. Flutamide reduced male courtship activity for one week, but display behavior then increased after two weeks of flutamide treatment. Our studies show that androgens modulate male manakin courtship, but the amount of courtship is not directly correlated with the concentration of circulating T. These results suggest that the relationships between androgen and courtship might differ between tropical and temperate birds.     

Social Control and Physiological Cost of Cheating in Status Signalling Male House Sparrows (Passer domesticus)

Flock-forming passerines often use plumage characteristics to signal their social dominance. While the benefits to signal dominance seem obvious, costs associated with status signalling are ambiguous. The social control hypothesis predicts that individuals of high social status – with large badges – are involved in more social interactions with individuals of similar badge size. Cheaters are therefore exposed to increased risk of fighting with high quality individuals and the costs associated with enhanced fights with dominant males are supposed to outweigh the benefits of cheating. We tested the social control hypothesis in male house sparrows ( Passer domesticus ), by observing social interactions in captive flocks and determining dominance relationships. Two low status individuals within each flock had the size of their badge experimentally increased and the interactions involving experimental and control birds were recorded. We also assessed the potential physiological cost of cheating in terms of enhanced levels of the stress hormone, corticosterone. Dominance was significantly positively correlated with badge size, but not with other morphological traits. We found little support for the social control hypothesis. Birds did not have significantly more interactions with individuals of similar badge size, before the manipulation. Similarly, after the experimental increase in badge size, experimental birds did not tend to have more encounters with large-badged males. Experimental birds with enlarged badges won more fights compared with prior to the manipulation, suggesting that badge size is used as a signal of social dominance even in small and stable flocks. Finally, corticosterone levels in the blood did not increase significantly after the manipulation of badge size, suggesting that there is no measurable cost, resulting from stress, in cheaters.     

Pre-breeding energy requirements: thyroid hormone, metabolism and the timing of reproduction in house sparrows Passer domesticus

We measured thyroid hormone (T3) levels and energy expenditure of pre-breeding house sparrows Passer domesticus in relation to the timing of breeding and reproductive success. The onset of reproduction was synchronised in two waves, separated by a three-week interval. On an annual basis, early breeders (birds that bred for the first time during the first wave) made significantly more breeding attempts, laid significantly more egg and raised 2.3 times more chicks to fledging than late breeders (birds that bred for the first time during the second wave). By the end of March, about one month before the first egg was laid in the population, plasma titres of testosterone in males and estradiol in females were still low and did not differ between early and late breeders. However, birds that subsequently bred early had higher titres of plasma triiodothyronine (T3) than birds that started to breed late. We show for the first time in a free-living bird population that Basal Metabolic Rate (BMR) is positively correlated with the plasma titre of T3. Differences in plasma T3 accounted for 48% of the inter-individual variation in BMR. Elevated T3 levels indicate that energy requirements increase prior to breeding. Although early breeding appears to be advantageous in terms of the number of offspring raised on an annual basis, the increased energy requirements prior to breeding are thought to delay the onset of reproduction in those birds that cannot afford the additional energy expenditure early in the season.     

Yolk hormones have sex-specific long-term effects on behavior in the pied flycatcher (Ficedula hypoleuca)

The hormonal environment during early development, such as maternally derived androgens in bird eggs, shapes the development and phenotype of the offspring in ways that may have important long-term consequences for behaviour. We studied the effects of yolk androgens on multiple behavioural traits in female and male pied flycatchers (Ficedula hypoleuca) by experimentally elevating androgen levels (testosterone and androstenedione) in the eggs. The birds were housed in a common-garden environment in captivity until full independence, after which their behaviour was tested. We found that androgen-treated males were more likely than control males to explore a novel environment and showed higher activity in the presence of a novel object. In response to a simulated predator attack, androgen-treated males mainly showed freezing behaviour, while control males showed escape behaviour. Females from the androgen treatment and control group showed no differences in these behaviours. Androgen treatment did not affect neophobia (latency to approach the novel object) or dominance behaviour in either sex. Behaviour in the novel environment and towards a novel object was repeatable, but behaviours in the different experiments were mostly not inter-correlated. These results indicate that yolk androgens have various long-lasting effects on behaviour, especially in males, but that they do not induce a distinct behavioural syndrome. As behaviour is strongly linked with fitness, our results suggest that yolk androgens may play a role in determining fitness, and thus play a potentially adaptive role.