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      Seasonal changes in courtship behavior, plasma androgen levels and in hypothalamic aromatase immunoreactivity in male free-living European starlings (Sturnus vulgaris).

      General and Comparative Endocrinology
      Androgens, blood, Animal Husbandry, Animals, Animals, Wild, Aromatase, metabolism, Behavior, Animal, physiology, Courtship, Dehydroepiandrosterone, Female, Hypothalamus, Immunohistochemistry, Male, Seasons, Starlings, Testosterone

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          Abstract

          In songbirds from temperate latitudes, singing during spring has an essential role in mate attraction, while during the non-breeding season it is connected to territorial aggression and/or maintaining dominance hierarchies or flock cohesion. Courtship behavior is regulated by plasma testosterone (T) levels. Other androgens, like dehydroepiandrosterone (DHEA) could be responsible for aggression. The aromatization of androgens in the brain is an essential step in mediating their effects on behavior. Our goal was to determine whether the seasonal changes in male courtship behavior (measured by average song bout length and wing-waving/flicking) are related to seasonal changes in androgen activity (measured by plasma T, DHEA levels) and aromatase (ARO) immunoreactivity in the preoptic area/medial preoptic nucleus (POA/POM) of free-living male starlings. DHEA increased during pair formation, decreased at nesting and remained at low levels. The number of ARO cells - in line with the T levels - increased during the courtship and nesting periods, but outside the breeding season it was low. Song bout length showed a similar pattern, namely the peak was reached during the courtship period, and after that males stopped singing when chicks started to hatch. Short and fast wing-flicking and wing-waving behavior was observed only during the breading season. Summarizing, we have found that song bout length of male starlings changes parallel with plasma T levels and ARO immunoreactivity in the POA/POM. Furthermore, DHEA levels were low during the sexually inactive period which suggests that other mechanisms could be involved in the aggressive non-courtship behavior/vocalization in these birds. Copyright © 2011 Elsevier Inc. All rights reserved.

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          Most cited references41

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          Regulation of territorial behavior in the sedentary song sparrow, Melospiza melodia morphna.

          Male song sparrows (Melospiza melodia morphna) of western Washington State show year-round territoriality. Although territorial aggression during the breeding season was accompanied by high circulating levels of luteinizing hormone (LH) and testosterone (T), similar aggression in the non-breeding season occurred when gonadal hormone levels were basal. Experimental removal of territorial males in autumn resulted in new males taking over the territory within a few days. These males had basal levels of LH and T despite establishing a new territory and the accompanying high level of aggression. There was also no difference in plasma levels of corticosterone in replacement versus established territorial males suggesting that social stress was not a factor. To test the possibility that low levels of gonadal steroids, or potentially some gonadal hormone not measured here, might regulate territorial aggression in the non-breeding season, free-living male song sparrows were castrated in early autumn and their aggressive territorial behavior was quantified by a simulated territorial intrusion (STI). Castrates showed the same aggressive responses to STI as controls indicating that establishment and maintenance of a territory was not dependent upon hormones of gonadal origin. Castrated males retained territories throughout the autumn and winter and even into the following breeding season. Further experiments were conducted to establish a role, if any, for T in territorial behavior in this species. During the breeding season when males had high levels of T, the responses to STI continued after the stimuli (caged conspecific male and tape-recorded songs) were withdrawn. Some males continued to patrol the territory and sang for long periods after STI. In contrast, males exposed to STI in autumn showed a strong aggressive response during the challenge, but then territorial aggression abated rapidly when the stimuli were withdrawn. Implants of T into males in autumn reinstated the high level of aggression after withdrawal of STI in a manner similar to that seen during the breeding season. These data suggest that in M. m. morphna T does not activate territorial aggression per se, but may increase the intensity of an aggressive response to STI, and persistence of the behavior after STI is withdrawn.
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            Novel mechanisms for neuroendocrine regulation of aggression.

            In 1849, Berthold demonstrated that testicular secretions are necessary for aggressive behavior in roosters. Since then, research on the neuroendocrinology of aggression has been dominated by the paradigm that the brain receives gonadal hormones, primarily testosterone, which modulate relevant neural circuits. While this paradigm has been extremely useful, recent studies reveal important alternatives. For example, most vertebrate species are seasonal breeders, and many species show aggression outside of the breeding season, when gonads are regressed and circulating testosterone levels are typically low. Studies in birds and mammals suggest that an adrenal androgen precursor-dehydroepiandrosterone (DHEA)-may be important for the expression of aggression when gonadal testosterone synthesis is low. Circulating DHEA can be metabolized into active sex steroids within the brain. Another possibility is that the brain can autonomously synthesize sex steroids de novo from cholesterol, thereby uncoupling brain steroid levels from circulating steroid levels. These alternative neuroendocrine mechanisms to provide sex steroids to specific neural circuits may have evolved to avoid the "costs" of high circulating testosterone during particular seasons. Physiological indicators of season (e.g., melatonin) may allow animals to switch from one neuroendocrine mechanism to another across the year. Such mechanisms may be important for the control of aggression in many vertebrate species, including humans.
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              Understanding the Complex Song of the European Starling: An Integrated Ethological Approach

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