Social stimuli, testosterone, and aggression in gull chicks: support for the challenge hypothesis

We tested the challenge hypothesis for the hormonal regulation of aggression in chicks of the black-headed gull, Larus ridibundus. Chicks of this species are highly aggressive toward conspecifics, but never to peers that hatched from the same clutch (modal clutch size is three). Therefore, in the first experiment small families were housed together in large groups (challenged condition) and compared to families kept isolated (nonchallenged condition). As expected, in the challenged condition during the initial stage of territory establishment basal levels of testosterone (T) were clearly higher than those in the nonchallenged condition. In the second experiment we tested the effect of a short social challenge on short-term T-fluctuations. The design was based on an earlier experiment, showing that after temporary T-treatment chicks become very sensitive to social challenges while having low basal T-levels. We now show that these social challenges induce brief elevations in plasma T-levels. These peaks are similar to those in previously untreated chicks but untreated chicks do not respond with aggression to a challenge. Therefore, we conclude that the initial exposure to elevated T-levels increases the sensitivity to brief changes in T induced by social challenges. In this way exposure to T, that may be detrimental for development, is minimized while birds remain able to defend territories. This is the first report showing that the challenge hypothesis as established for adult birds, is also applicable for aggressive behavior in young birds outside the sexual context. Furthermore we suggest that a phase of priming with T is necessary to obtain the high behavioral responsiveness to a challenge.     

The relationships among testosterone, conditioned aggression, and dominance in male pigeons

Pigeons lowest in their homeloft dominance hierarchies were either injected with testosterone, conditioned to peck the more dominant birds, or both, and were then returned to their homelofts. Frequency of pecks and threats received by each animal was recorded. Testosterone alone had no effect. Conditioned birds were pecked significantly fewer times after treatment. The combination of hormone treatment and conditioning produced the greatest enhancement in dominance. Differences in the patterns of fighting behavior are noted and results are discussed in a discrimination learning framework as an interaction between androgen and learned responses.     

Female testosterone, dominance rank, and aggression in an Ethiopian population of hybrid baboons

Studies on the relationship between female testosterone (T) measures and behavior, particularly in free-ranging primate populations, remain scant. In this study we used fecal steroid analysis to examine the effects of seasonal, reproductive, and social factors on female T in a group of free-ranging hybrid baboons (Papio sp.) in the Awash National Park of Ethiopia. We collected behavioral and hormonal data from 25 adult females across an 11-month period. Solid phase extraction and radioimmunoassay (RIA) techniques were used to quantify T in 776 fecal samples collected weekly from each female. The results indicate that 1) the females had elevated T during pregnancy and during the wet season relative to other periods, 2) female dominance rank was positively related to T measures, and 3) female T and aggression were positively related within subjects but not across subjects. Higher T concentrations during pregnancy are consistent with other published profiles of pregnancy in primates. In combination with data on foraging, wet season increases in T may indicate contest competition for females. The rank-T relationship may be mediated by supplants or aggression. Finally, we discuss the different interpretations of the hormone-behavior relationship based on within- and across-subject analyses.     

Effects of testosterone on song, aggression, and nestling feeding behavior in male great tits, Parus major

As outlined in the trade-off hypothesis of testosterone (T) secretion, fluctuations in T during the breeding season might reflect how males allocate their time and energy to competitive behaviors for mates and territories, associated with high T levels, and parental activities, associated with low T levels. In the present study, great tit, Parus major, males were implanted with T-filled or empty silastic capsules at the start of the breeding season and the behavior of these two male categories was compared during the entire breeding season. As a measure of competitive behavior we looked at song behavior and territorial responsiveness to a male decoy, during the three main stages of the breeding period (the egg-laying, incubation, and nestling stages). As a measure of parental care we looked at feeding behavior during the nestling stage. Our results only partly supported the trade-off hypothesis. T implants increased plasma androgen levels and enhanced spontaneous song activity and the production of aggressive vocalizations in response to a decoy. However, our results suggest that the degree of physical aggression might be less than fully coupled with T. First, approach to the decoy was not affected by the treatment. Second, although T levels are known to vary from high during egg laying to low while feeding young, control and T-treated males spent similar amounts of time close to the decoy in the three breeding stages. Our results thus suggest that vocal and physical aggression might be regulated differently in the great tit. Furthermore, in contrast with most other studies on temperate bird species but in agreement with a previous study on the great tit, T treatment did not affect male feeding rates. As the dose of T we used was lower than that typically used in other studies, we cannot at present completely exclude the possibility that the latter result reflects this lower dose of T rather than the species used.     

The dose-response to testosterone propionate of preputial glands, pheromones and aggression in mice

Urine from female mice injected with 24 daily doses of 0, 1, 10, 50, and 100 μg testosterone propionate (TP) was applied to the coat of castrate males, and the aggressive response of fighter mice toward these castrates recorded. Some antiaggressive property in castrate female urine was confirmed, and this was neutralized by only 1 μg daily TP. Urine from the 50 μg group greatly increased the aggression response, but 100 μg had no additional effect.     

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.     

Arachidonate-induced thrombosis in mice: effects of gender or testosterone and estradiol administration

Sodium arachidonate (i.v.) has previously been shown to induce pulmonary emboli formation and a dose dependent cyanosis and respiratory depression in mice. Subsequently, we found that male mice are significantly more sensitive to arachidonate than females. Aspirin given orally 2 hours prior to arachidonate administration inhibits the responses of both males and females. Pretreatment with depo-testosterone markedly increases the effect or arachidonate in both males and females and depo-estradiol pretreatment reduces the responses in all mice. This exacerbation by testosterone of the arachidonate response and the attenuating effects of estradiol is consistent with data reported using other thrombogenic techniques.     

Autumnal territorial aggression is independent of plasma testosterone in mockingbirds

Mockingbirds (Mimus polyglottos) show intense territorial activity in the autumn as newcomers attempt to establish space within resident populations. Examination of autumnal territorial behavior showed that unmated males sing more and engage in more territorial fights than mated males. Newcomers that have just acquired space also sing more and show more territorial fights than birds resident to the population for at least one prior season. Among established residents, the average number of territorial fights was greater in birds that shared more territory boundaries with new residents. Radioimmunoassay of plasma samples taken from males during the molt and following the onset of territorial defense showed that during both periods plasma concentrations of testosterone (T), dihydrotestosterone (DHT), and estradiol were basal or below the sensitivity of the assay system. Moreover, groups of males that differed in song and territorial aggression did not differ in plasma concentrations of T, DHT, or luteinizing hormone (LH). Hormone analyses confirm measurements on several other avian species suggesting that sex steroid concentrations are low in the fall and winter and that variations in aggressive behavior at this time of year may be unrelated to LH and androgen levels. Our observations contribute to a growing body of work in temperate passerines indicating that the role of androgens in mediating aggressive challenge may be restricted to the breeding season. The possible hormonal basis (if any) of song and territorial aggression in mockingbirds outside the breeding season remains obscure.     

Salivary testosterone and aggression, delinquency, and social dominance in a population-based longitudinal study of adolescent males

Testosterone (T) has been found to have a stimulating effect on aggressive behavior in a wide range of vertebrate species. There is also some evidence of a positive relationship in humans, albeit less consistently. In the present study we investigated the relationship between T and aggression, dominance and delinquency over time, covering a period from early adolescence to adulthood. From a large population-based sample (n = 1.161) a subgroup of 96 boys was selected whose behavior had been assessed repeatedly by different informants from age 12 to 21 years, and who had provided multiple T samples over these years of assessment. On the whole, a decrease in aggressive and delinquent behavior was observed in a period in which T rises dramatically. Boys who developed a criminal record, had higher T levels at age 16. In addition, positive associations were observed between T and proactive and reactive aggression and self-reported delinquent behavior. Over the pubertal years different forms of aggressive and delinquent behavior were positively related to T, which may indicate that specific positive links are dependent on the social setting in which this relationship is assessed.     

Maternal testosterone in tree swallow eggs varies with female aggression

Variation in the investment of maternal resources in eggs, such as proteins and lipids, can have a profound influence on the growth and development of young. Maternal resources transferred to eggs also include androgens found in the yolk. In several species of birds the concentration of testosterone in the yolk either increases or decreases with laying order. Yolk testosterone has been shown to have various effects on the young including enhanced growth and dominance as well as reduced survival. Previous work suggested that the concentration of testosterone in the yolk may be influenced by the female's social conditions, specifically the frequency of aggressive interactions. In tree swallows, Tachycineta bicolor, we found that yolk testosterone was correlated with the aggressive interactions of the female before and during egg laying. In contrast to other species, yolk testosterone did not vary with laying order in tree swallows. Thus, patterns of yolk testosterone are more variable than thought previously and may be influenced by the social conditions experienced by the female during laying.     

Relationships between aggression and pubertal increases in testosterone: A panel analysis of adolescent males

Abstract

Existing data linking testosterone (T) and aggression in human adult males are surprisingly tenuous. In one of the few studies based on adolescent males, Olweus et al. (1988) demonstrated strong relationships between concurrent measures of T and aggression. However, the conclusions that could be drawn regarding developmental change were limited. Using data from a three‐year panel study of 100 adolescent males (ages 12 to 13 at study entry), we examined whether there are significant relationships between concurrently collected measures of T and self‐ratings of aggression, and whether the dramatic pubertal rise in T predicts subsequent change in aggression ratings. Panel analyses incorporating concurrent, lagged, and change measures found few significant relationships between aggression and T or pubertal development. The general absence of T/aggression relationships is discussed in the context of other empirical findings, the aggression measures used, and prepubertal differentiation on aggression.     

Fear of dogs in a community sample: Effects of age,gender and prior experience of canine aggression

Abstract

An investigation was conducted into human fear of dogs and experiences of canine aggression in an adult community sample (n = 292). Consistent with expectations, it was found that, while fear of dogs was relatively common (present in almost half the respondents), fear of dog attacks was less so, and extreme fear of dog attacks was very rare. Women, middle-aged and older adults were more likely to fear dogs than men and younger adults, while older people were more likely than younger ones to fear dog attacks. Reported encounters with canine aggression, particularly threatening behavior, were relatively common, but having been attacked by a dog was less strongly related to fear of dogs than having been threatened by a dog. Logistic regression analyses revealed that being female, having been threatened by a dog, and being older were strong predictors of dog-related fear, while being older and obtaining higher scores on a measure of trait anxiety predicted fear of dog attacks.     

The effects of castration and Silastic implants of testosterone on intermale aggression in the mouse

Castration and testosterone (T) replacement were used to study developmental changes in aggressive behavioral responsiveness to androgenic stimulation. Male mice castrated at birth were less sensitive to circulating T than were prepubertal or adult castrates, but fighting was induced in neonatal castrates with a dose of androgen that produced hypertrophy of the accessory organ system in adult castrates. Gonadectomy shortly prior to pubertal increases in serum T concentration also reduced behavioral responsiveness to androgen administration. Intermale aggression was induced in prepubertal castrates only with T treatment that maintained accessory organ growth in adult castrates. The aggressive behavior of males castrated after the pubertal surge in serum T was supported with circulating levels of androgen that failed to stimulate the accessory organ system above that of oil-treated castrates. It was concluded that T stimulation during neonatal or pubertal life is not totally crucial for organization of neural substrates that mediate the ultimate expression of intermale aggression, but exposure to androgen from birth throughout pubertal development is normally required to produce maximal aggressive behavioral responsiveness to circulating T encountered in adulthood.     

Dominance and prestige as differential predictors of aggression and testosterone levels in men

The relationship between self-esteem and aggression has yielded mixed results and generated much recent debate in the social psychology literature. Based on an evolutionary-psychological theory of self-esteem, Kirkpatrick et al. [Kirkpatrick, L. A., Waugh, C. E., Valencia, A., Webster, G., 2002. The functional domain-specificity of self-esteem and the differential prediction of aggression. Journal of Personality and Social Psychology 825, 756–767] showed that multiple, functionally distinct self-esteem mechanisms predict aggression differentially: e.g., “self-perceived superiority” is positively related, and “social inclusion” inversely related, to behavioral aggression. The present study extends this research by further differentiating two distinct forms of “superiority,” dominance and prestige [Henrich, J., Gil-White, F. J. 2001. The evolution of prestige: Freely conferred deference as a mechanism for enhancing the benefits of cultural transmission. Evolution and Human Behavior 22, 165–196], in the prediction of aggression in men and women and testosterone levels (measured in saliva samples) in men. Dominance was positively related, but prestige was either unrelated or inversely related, to self-report aggression measures. Dominance was unrelated but prestige inversely related to testosterone levels in men, perhaps suggesting a method of testosterone inhibition in individuals attaining prestige-based superiority. In addition to contributing to the growing literature on the aggression–self-esteem link, the results provide validation for the prestige–dominance distinction and support, but also suggest an important refinement to, a theory of self-esteem as a collection of functionally distinct adaptations.     

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.     

Serum testosterone, male dominance, and aggression in captive groups of vervet monkeys (Cercopithecus aethiops sabaeus)

The relationship of serum testosterone concentration to male dominance rank and frequency of aggression was investigated in stable vervet monkey social groups, each containing two or three adult males, several adult females, and their offspring. Dominance relationships were determined by noting an animal's success in intermale aggressive encounters. A striking finding was the marked within-subject variation in testosterone concentration: 5- to 10-fold fluctuations were often observed on successive days. When all 15 groups were considered together, testosterone concentration was unrelated to dominance rank. Although mean testosterone concentration for all dominant males was higher than the mean for all subordinate males, this difference was not significant. In a subset of 4 groups, the rate of aggression initiated was significantly correlated with same-day testosterone in dominant but not in subordinate males.     

Context matters: female aggression and testosterone in a year-round territorial neotropical songbird (Thryothorus leucotis)

Testosterone promotes aggressive behaviour in male vertebrates during the breeding season, but the importance of testosterone in female aggression remains unclear. Testosterone has both beneficial and detrimental effects on behaviour and physiology, prompting the hypothesis that selection favours an association between aggression and testosterone only in certain contexts in which intense or persistent aggression may be beneficial. We tested this hypothesis in a year-round territorial female buff-breasted wrens (Thryothorus leucotis), by exposing free-living females to experimental intrusions in different social (either single female or male, or paired decoys) and seasonal (pre-breeding or breeding) contexts. Females responded more aggressively to intrusions by females and pairs than to males. However, female intrusions elicited stronger responses during pre-breeding, whereas responses to pair intrusions were more intense during breeding. Territorial females had elevated testosterone levels after female intrusions and intermediate levels after pair intrusions during pre-breeding, but the levels of testosterone remained low after these intrusions during breeding. These results demonstrate seasonal differences in circulating testosterone following territorial aggression in female buff-breasted wrens and are suggestive of differences according to social context as well. Context-dependent elevation of testosterone implies that selection acts directly on female vertebrates to shape patterns of testosterone secretion.     

Preliminary evidence that testosterone's association with aggression depends on self-construal

A contribution to a special issue on Hormones and Human Competition.Previous research and theory suggest testosterone is an important hormone for modulating aggression and self-regulation. We propose that self-construal, a culturally-relevant difference in how individuals define the self in relation to others, may be an important moderator of the relationship between testosterone and behaviors linked to aggression. Within two studies (Study 1 N = 80; Study 2 N = 237) and an integrated data analysis, we find evidence suggesting that acute testosterone changes in men are positively associated with aggressive behavior for those with more independent self-construals, whereas basal testosterone is negatively associated with aggression when individuals have more interdependent self-construals. Although preliminary, these findings suggest that self-construal moderates the association between testosterone and aggression, thereby paving the way toward future work examining the potential cultural moderation of the behavioral effects of testosterone.     

Effects of intracranial implants of testosterone propionate on intermale aggression in the castrated male mouse

Three experiments were conducted in order to assess the effects of intracranial implants of testosterone propionate (TP) on intermale aggression in the castrate male CF-1 mouse. In Experiment 1, seven groups received bilateral implants containing a total of 27 μg crystalline TP into the septum, neocortex, lateral ventricles, preoptic-anterior hypothalamus, hippocampus, medial reticular formation, and subcutaneously, and were tested 2 and 4 days after treatment. An eighth group received blank pellets in the brain. Animals receiving septal or lateral ventricle implants fought significantly more than other groups on trial 1. This difference had disappeared by trial 2, indicating diffusion of the hormone. The diffusion was corroborated by significant seminal vesicle growth. In Experiment 2 animals received bilateral implants of a total of 4.5 μg TP in paraffin or a blank pellet into the septum, preoptic-anterior hypothalamus, cortex, amygdala, olfactory bulbs, medial reticular formation, or subcutaneously. None of these treatments proved effective for activating aggression. Experiment 3 explored the activational effects of 10 μg of TP implanted bilaterally into the same areas as in Experiment 2, excluding the olfactory bulbs and cortex. Implants into the septum were followed by significantly increased fighting. Implants into the preoptic area were only marginally effective whereas the remaining two areas were not responsive to hormone treatment and did not differ from control animals. No seminal vesicle growth was detected as a result of the hormone treatments. These results would indicate that the septum is important in the control of androgen-dependent, intermale aggression in the male CF-1 mouse.