Simulated Territorial Intrusions Research Articles

Testosterone implants increase song but not aggression in male Lapland longspurs

Lapland longspurs,Calcarius lapponicusare tundra-nesting arctic birds with an extremely short breeding season. Males show a pronounced brief peak of plasma testosterone early in the season. We studied the effect of exogenous testosterone on song and aggression in free-living male Lapland longspurs. We gave high-testosterone implants to 16 birds, low-testosterone implants to seven birds, and empty or no implants to 33 birds. The implants resulted in significantly different plasma testosterone levels during incubation (high-testosterone mean=20.79±3.4ng/ml, low-testosterone mean=2.54±0.5ng/ml, control mean=0.53±0.1ng/ml). High-testosterone birds had larger cloacal protuberances than controls, but low-testosterone birds did not. We measured aggression and song with simulated territorial intrusions during incubation, a mean of 12.03±1.45 days after the insertion of implants. High-testosterone birds and low-testosterone birds were no more aggressive than controls. However, high-testosterone birds, but not low-testosterone birds, were significantly more likely than controls to sing. These results suggest that the high, brief testosterone peak of Lapland longspurs may be related more to song than to territorial aggression. Alternatively, both aggression and song may be testosterone-influenced, but aggression may be more readily suppressed during incubation. The hormone-behaviour patterns demonstrated in this study may be adaptations for breeding in the short arctic summer.

Temporal Patterns of Territorial Behavior and Circulating Testosterone in the Lapland Longspur and Other Arctic Passerines

We studied territorial aggression in relation to circulating testosterone levels in free-living birds of four species in northern Alaska. The Lapland longspur, Calcarius lapponicus , is an abundant breeding passerine on the arctic tundra. Unlike many passerines at lower latitudes, male Lapland longspurs do not defend a “multiple-purpose territory” that serves to provide nest sites, food and shelter. Rather, after arrival on the breeding grounds, they perform aerial display flights over a loosely denned “nest area” for a very brief period of two days or so, showing tolerance of other males. This song display may be involved in courtship. During this phase, male longspurs show a brief and pronounced peak in circulating testosterone levels, and are not aggressive toward simulated territorial intrusions (STIs). Males then “guard” their sexually receptive mates for about ten days, during which they are highly aggressive toward STIs, but do not sing as much. During the next phase, incubation, the males become very tolerant of conspecific males. Their circulating testosterone levels decline to baseline levels, and they generally do not sing or display aggression in response to STIs. Three other passerines, the white-crowned sparrow, Zonotrichia leucophrys gambelii , American tree sparrow, Spizella arborea , and savannah sparrow, Passerculus sandwichensis , show patterns of territorial aggression typical of species studied at lower latitudes. Welldefined territories are defended for several weeks, during which there is a prolonged peak in plasma concentrations of testosterone. These three species continue to sing and display aggression even late in the season, unlike the longspurs. The peak of testosterone in the longspurs occurs simultaneously with the peak in song display, while in mid-latitude species it occurs with the peak in reproductive aggression. These data suggest that the interrelationship of testosterone and aggression in Lapland longspurs may be different from that of passerines with multiple-purpose territories, and may be related to the constraints of breeding in the open arctic tundra.

Behavioral and Hormonal Responses of Male Song Sparrows to Estradiol-Treated Females during the Non-breeding Season

Previous studies on several species have shown that behavior of female vertebrates given estradiol implants to maintain sexual receptivity resulted in elevated levels of testosterone in males and even delayed termination of breeding in their otherwise untreated mates. However, the efficacy of such treatment in the nonbreeding season was unclear. In this study, female song sparrows, Melospiza melodia morphna, given implants of estradiol in autumn showed elevated sexual behavior—especially "chitters," a loud, female-specific vocalization used mostly during the breeding season. Males in autumn appeared to ignore the sexual behavior of these females, showed no difference in response to simulated territorial intrusion, and bad basal circulating levels of testosterone when compared with males tested in an area of control females. However, by late winter (February) males in the area where females were treated with estradiol had elevated levels of testosterone compared to control males and those of both groups sampled in autumn. These data indicate that sexual behavior of females, experimentally induced by estradiol implants, failed to increase sexual and territorial behavior in males during the autumn. On the other hand, reproductive behavior of females did appear to accelerate the vernal increase in testosterone concentrations in blood of males.

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.

Testosterone and territorial behaviour in sedentary and migratory sparrows

Abstract. Free-living male song sparrows, Melospiza melodia morphna, showed marked aggressive behaviour in response to simulated territorial intrusions throughout most of the year. Only during the prebasic moult, and during inclement winter weather, was territorial aggression suppressed. In contrast, free-living male white-crowned sparrows, Zonotrichia leucophrys pugetensis , showed the highest behavioural responses to simulated territorial intrusions in spring when territories were established. Responses then declined as the breeding season progressed, reaching a minimum during the prebasic moult. The latter species migrates to wintering grounds and does not show territorial aggression until the following spring. Plasma levels of testosterone paralleled changes in territorial aggression in white-crowned sparrows, but not song sparrows. The resurgence of autumnal territoriality was independent of any increase in circulating testosterone levels. Males of both species showed increases in testosterone levels in response to simulated territorial intrusions, but this was only significant in white-crowned sparrows. However, male song sparrows had higher levels of testosterone in spring in areas with a high density of territories than males in areas with a low density of territories. These data suggest that although territorial behaviour in the non-breeding season was independent of testosterone in song sparrows, such behaviour in the breeding season may be influenced by this steroid hormone. Finally, it appears that young, first summer, song sparrows were also able to establish a territory in early autumn with no changes in testosterone or luteinizing hormone.

Territorial Aggressiveness and Its Relation to the Endocrine System in the Pied Flycatcher

Behavioral and endocrine responses were studied following simulated territorial intrusions performed at two different stages in the breeding cycle (pre-nest-building and nestling period) of the pied flycatcher (Ficedula hypoleuca). Only 45% of the unpaired territorial males from the pre-nest-building period defended their territories by attacking the decoy. After the experimental intrusion unpaired males attacking the decoy had significantly higher plasma testosterone levels than nonattacking unpaired males. Plasma corticosterone levels were significantly higher in both attacking and nonattacking unpaired males than in control males. There were no differences in body size between attacking and nonattacking males. The attacking paired males and paired control males, however, had significantly lower fat depots than other males. The endocrine system of the male pied flycatcher responded within 1 day to the settlement of a female in the territory in that plasma testosterone levels of paired control males were significantly higher than those in unpaired territorial control males. The proportions of attacking males increased significantly (up to 80%) once a female had settled. Unlike in unpaired territorial males, testosterone levels in paired males that attacked the decoy were similar to those in non-attacking males and to those in paired control males after a simulated territorial intrusion. Data suggest that the high testosterone levels are related to territorial aggressiveness and not to sexually related events such as mate-guarding or singing. Forty-five percent of the males from the nestling period did attack the decoy. Despite the strong behavioral response these attacks had no effects on plasma testosterone or corticosterone levels. As all males during the nestling period only have basal levels of testosterone, it is concluded that in the pied flycatcher, high testosterone levels are not necessary for the expression of an aggressive behavior at this stage in the breeding cycle. In the pied flycatcher aggression at this stage in the breeding cycle is likely only to be associated with the defense of food resources.

Hormonal and behavioural responses to simulated territorial intrusion in the cooperatively breeding white-browed sparrow weaver, Plocepasser mahali

Abstract. Behavioural investigations of stable groups of white-browed sparrow weavers indicate that they not only bred cooperatively, but also defended territories from other groups. Territory defence involved regular patrolling of boundaries plus a characteristic chorus vocalization that was given by all group members in concert. Song was performed exclusively by the breeding male and only during the breeding season. Territorial choruses were given by all members of the group at all seasons and could also be initiated by all members, although the breeding male and female initiated more choruses than helpers. Simulated territorial intrusions (achieved by placing a caged group within a territory and playing back tape-recorded choruses through a speaker placed alongside) resulted in dramatic increases in territorial aggression by all group members. Plasma levels of testosterone were not affected by the intrusions in breeding birds or helpers. However, plasma levels of luteinizing hormone were significantly elevated in the breeding females after challenge. These data are consistent with other observations in this species that territorial aggression is independent of circulating testosterone, but is correlated with luteinizing hormone. Corticosterone levels were higher in controls than in birds exposed to simulated territorial intrusions with the exception of breeding females. Although the significance of this latter result is unclear, it does seem likely that 'psychological castration' of non-breeders is not mediated through elevated circulating levels of glucocorticosteroids.

Behavioral, hormonal, and morphological responses of free-living male pied flycatchers to estradiol treatment of their mates

A field experiment was performed implanting female pied flycatchers ( Ficedula hypoleuca) during the nest-building period with silastic tubes containing 17β-estradiol. Control females were given empty silastic tubes. The pied flycatcher is a polygamous and polyterritorial bird species. During two successive breeding seasons effects on reproductive behavior and the reproductive systems of males were studied. Reproductive success was not affected by the treatment. Estradiol treatment of females caused marked changes in the behavior of males, increasing aggressive and mate-guarding behavior. The results of the present study also support the idea that cuckoldry is a problem for the territory holder. Fewer males paired with estradiol-treated females established secondary territories, and significantly more of the polyterritorial males from the experimental population showed up in the home-territory when a simulated territorial intrusion was performed there. Control males were much more successful in getting a second female to breed. Spermatogenesis and hormonal cycles (DHT, LH, and testosterone) in males were not prolonged as a result of estradiol treatment of the females.

Androgen control of social status in males of a wild population of stoplight parrotfish, Sparisoma viride (Scaridae)

In the protogynous stoplight parrotfish ( Sparisoma viride), large males defend territories that encompass the home-ranges of several mature females. However, high-quality habitat is in short supply, such that smaller, competitively inferior males do not defend territories. We investigated the role of 11-ketotestosterone (11KT) and testosterone (T) in the regulation of territorial behavior in a wild population of a protogynous reef fish, the stoplight parrotfish, at Glover's Reef, Belize. Radioimmunoassay of plasma samples from individuals of known social status revealed that nonterritorial males have lower levels of T and 11KT than territorial males. Nonterritorial males allowed access to vacant territories underwent pronounced increases in T and 11KT. When sampled 1 week after territory acquisition, levels of T and 11KT in new territorial males were significantly higher than the levels in established territorial males, but by 3 weeks after territory acquisition, there was no significant difference. We further investigated the hypothesis that such short-term increases in androgen levels are a response to intense male-male interactions during territory establishment. Simulated territorial intrusion promoted increased plasma levels of both T and 11KT while access to vacant territories without neighboring territorial males did not. These findings suggest that the endocrine system plays a role in fine-tuning the levels of territorial aggression exhibited by male stoplight parrotfish. We discuss these results in light of recent theory in behavioral endocrinology.

Endocrine Response of Captive Male Brown-Headed Cowbirds to Intrasexual Social Cues

The hormonal response to a spectrum of intrasexual social stimuli was studied in captive Brown-headed Cowbirds (Molothrus ater). Males were housed in individual cages in one of four conditions: (1) in a semicircle with other males (= visual + vocal stimuli), (2) in acoustic chambers with visual access to a devocalized companion (= visual stimuli only), (3) in chambers in which a tutor tape was played daily (= vocal stimuli only), and (4) in acoustic chambers with no other input (neither visual nor social stimuli). Blood samples were taken at 2-week intervals throughout the spring and early summer and assayed for testosterone. The results indicate that the greatest increase in testosterone was in the birds receiving visual plus vocal stimuli and in those receiving only visual stimuli; males receiving only vocal stimuli had a muted endocrine response, and those receiving no social stimulation exhibited the briefest response. The relatively small response to vocal stimulation is consistent with the absence of a behavioral response to simulated territorial intrusions (i.e., song playbacks) that has been shown in previous studies in male cowbirds.

Changes in plasma levels of testosterone during male-male interactions in the song sparrow, Melospiza melodia: time course and specificity of response

Previous investigations have shown that malemale interactions over territory boundaries result in an increase in plasma levels of testosterone (T). In order to determine the time course of this increase following an agonistic challenge, male song sparrows, Zonotrichia (= Melospiza) melodia, were exposed to simulated territorial intrusions. Responding males were captured at intervals after onset of the intrusion for up to 60 min. Plasma levels of T were elevated by 10 min after onset of the challenge, and remained high in birds sampled 10–60 min after onset of the intrusion. In addition, plasma levels of luteinizing hormone (LH) increased and were significantly elevated after 10 min of stimulation. The results suggest that at least the prolonged elevation of T secretion precipitated by a male-male interaction was mediated via an increase in LH release. However, the initial surge of T levels in plasma may be LH independent. p Investigations of captive birds confirmed that circulating LH and T levels increased when male song sparrows were challenged by a conspecific male. Challenges involving a male house sparrow, Passer domesticus, had no effect suggesting that responses to male intrusions were species characteristic and not a result of general arousal. Further, auditory stimuli (vocalizations) alone, and visual stimuli (a devocalized male) alone were less effective in stimulating an increase in secretion of T than a combination of auditory and visual stimuli.

Territoriality and monogamy among agile gibbons (Hylobates agilis)

I simulated territorial intrusions by mated pairs, solitary males and solitary females through song playback to investigate the behaviors that agile gibbons (Hylobates agilis) use to maintain territoriality and monogamy. Mated male and female gibbons approached and duetted in response to a simulated territorial intrusion by a neighboring group. Strange solitary females elicited similar approach and singing responses from mated pairs. In contrast, the simulated presence of a solitary male consistently evoked approaches by mated males only. Females and males did not contribute equally to pair movements or to answering songs; males led the majority of approaches, while females initiated all duets. I hypothesize that carrying small, vulnerable infants may inhibit females from leading approaches. These results are consistent with previous studies which suggest that female territoriality prevents male gibbons from becoming polygynous.

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 testostrone 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.