Female marmosets' behavioral and hormonal responses to unfamiliar intruders

The endocrine control mechanisms for female mammalian aggression have been largely unstudied. Although it has been proposed that androgens may modulate female aggressive behavior in a similar manner to males, very little conclusive evidence exists. Previous work in male marmosets found that post‐encounter increases in testosterone (T) were dependent on the intensity of aggression displayed during the aggressive encounter. We exposed female marmosets (Callithrix kuhlii), a monogamous and biparental primate, to aggressive interactions with unfamiliar intruders. Individual female marmosets exhibited changes in T and estradiol (E₂) that are associated with aggressiveness dependent on the intensity of aggression displayed as well as their role during the encounter. Resident females exhibited increased E₂ immediately following an encounter in which they displayed high rates of aggression. If resident females received high rates of aggression from the intruder, the resident displayed increased T 24 hr following the encounter. Interestingly, if the female was an intruder in the encounter, the intensity of her aggression was associated with increased cortisol immediately following the trials, whereas received aggression was associated with increased T and E₂ immediately following the trial. Female primates do exhibit situation‐dependent changes in gonadal steroids in association with aggression that may serve to prime them for future aggressive interactions. Am. J. Primatol. 73:1072–1081, 2011. © 2011 Wiley‐Liss, Inc.     

Females competing to reproduce: dominance matters but testosterone may not

The associations among aggression, testosterone (T), and reproductive success have been well studied, particularly in male birds. In many species, males challenged with simulated or real territorial intrusions increase T and levels of aggression, outcomes linked to higher dominance status and greater reproductive success. For females, the patterns are less clear. Females behave aggressively towards one another, and in some species, females respond to a social challenge with increases in T, but in other species they do not. Prior work on female dark-eyed juncos (Junco hyemalis) had shown that experimental elevation of T increases social status and intrasexual aggression. Here, we conducted two experiments designed to answer three questions: Are endogenous concentrations of T associated with dominance status in captive female juncos? Does dominance status influence readiness to breed in female juncos? And do captive females increase T in response to a challenge? In the first experiment, we introduced two females to a breeding aviary, allowed them to form a dominance relationship and then introduced a male. We found that dominant females were more likely to breed than subordinates, but that dominance status was not predicted by circulating T. In the second experiment, we allowed a resident male and female to establish ownership of a breeding aviary (territory) then introduced a second, intruder female. We found that resident females were aggressive towards and dominant over intruders, but T did not increase during aggressive interactions. We suggest that during the breeding season, intrasexual aggression between females may influence reproductive success, but not be dependent upon fluctuations in T. Selection may have favored independence of aggression from T because high concentrations of T could interfere with normal ovulation or produce detrimental maternal effects.     

Circulating steroid hormones during rapid aggressive responses of territorial male mountain spiny lizards, Sceloporus jarrovi

Levels of aggression and circulating steroid hormones were monitored simultaneously in free-living male lizards following a staged territorial aggressive encounter with another male. In the first 15 min following the aggressive encounter, the frequency of territorial patroling and the frequency of agonistic and advertisement displays increased four- to fivefold in resident males. In most cases these increases persisted for at least 90 min after withdrawal of the intruder male and probably persisted for the entire day of the encounter. Blood samples collected at 15-min intervals revealed no changes in circulating levels of testosterone or corticosterone while this behavioral change was occurring. Thus, the increase in aggressive behavior that follows a male-male territorial encounter in this species does not appear to be mediated by simultaneous changes in circulating levels of these hormones. Interspecific comparisons suggest that interspecific variation in steroid hormone involvement in rapid aggressive responses may depend on the mating system and the extent of male parental care.     

The hormonal response of female European Stonechats to a territorial intrusion: the role of the male partner

In many bird species, the female participates in defending a pair's breeding territory, however, the endocrine control mechanism of female aggressive behavior is largely unknown. The general statement that androgens are involved in the regulation of aggressive behavior is based on studies conducted only in males. Here, we tested whether paired female stonechats show a hormonal response to a simulated male territorial intruder. Since in males of territorial bird species androgen levels usually increase following a male-male encounter, we measured androgen-levels before and after a simulated male intrusion. In addition, we measured estradiol, the main gonadal hormone in females, and corticosterone, a stress hormone. The results show that a male intruder does not affect any of the measured hormones in females. In a second experiment, we also tested whether the endocrine state of the male partner affects the hormonal response of females to a male intruder by comparing the hormonal response of females paired with pharmacologically castrated males and females paired with control males. Females paired with pharmacologically castrated males had lower corticosterone levels both before and after the intrusion than females paired with control males. Additionally, in both groups, female corticosterone levels were increased following a male intrusion. We suggest that the differences found between females paired with pharmacologically castrated males and females paired with control males are due to differences in intra-pair interactions.     

Inter-male aggression with regard to polygynous mating system in Pampean grassland mouse, Akodon azarae (Cricetidae: Sigmodontinae)

Based on the hypothesis that, in Akodon azarae, polygyny operates through female defence, we studied inter-male aggression in order to test the following predictions: during the breeding period (1) resident males are more aggressive than intruder males in the presence of females (FP), and (2) aggressive behaviour is independent of male condition (resident or intruder) in the absence of females (FA). To test our predictions, we used the resident male behavioural response towards an intruder male in relation to FP or FA. We conducted 30 encounters in FP and 27 in FA in 0.79-m² round enclosures placed in the Espinal Reservation. Our results support the prediction that, in FP, the intensity of aggressive behaviour exhibited by males varied in relation to resident or intruder condition. Resident males showed high levels of aggression towards intruders, and intruders exhibited the greatest values of submissive behaviours with residents. In FA, the intensity of aggressive behaviour did not vary in relation to resident or intruder condition. Both resident and intruder males exhibited low aggressive behaviour and inter-male encounters resulted mainly in non interactive behaviours. Our results support the hypothesis that, in A. azarae, the polygynous mating system operates through female defence.     

Sex Differences in Territorial Behavior Exhibited by the Spotted Hyena (Hyaenidae, Crocuta crocuta)

Spotted hyenas ( Crocuta crocuta ) are gregarious carnivores that defend group territories against encroachment by neighboring conspecifics. Here we monitored the behavior of members of one clan of free-ranging spotted hyenas during border patrols, 'wars' with neighboring clans, and other interactions with alien intruders, to document differences between the sexes in territorial behavior in this species. We also examined the possibility that the probability or rate of attack on alien hyenas encountered within the clan's territory would vary with the sex of the intruders. Initiation and leadership of most cooperative territorial behaviors were by adult female clan members, although border patrols were occasionally conducted by groups composed exclusively of resident males. The vast majority of alien intruders into the territory of the study clan were males. Resident females were more likely to attack intruding females than intruding males, but hourly rates of aggression directed by females towards aliens did not vary with intruder sex. Resident males were more likely than resident females to attack alien males, and resident males directed significantly higher hourly rates of aggression towards intruding males than females. Although female leadership in most cooperative territorial behaviors distinguishes spotted hyenas from many mammalian carnivores, other sex differences in the territorial behavior of spotted hyenas resemble those documented in other gregarious predators. Sex differences observed in hyena territoriality are consistent with the hypothesis that male and female clan members derive different selective benefits from advertisement and defense of group territories.     

Maternal aggression in endothelial nitric oxide synthase-deficient mice

Lactating female rodents protect their pups by expressing fierce aggression, termed maternal aggression, toward intruders. Mice lacking the neuronal nitric oxide synthase gene (nNOS-/-) exhibit significantly impaired maternal aggression, but increased male aggression, suggesting that nitric oxide (NO) produced by nNOS has opposite actions in maternal and male aggression. In contrast, mice lacking the endothelial nitric oxide synthase gene (eNOS-/-) exhibit almost no male aggression, suggesting that NO produced by eNOS facilitates male aggression. In the present study, maternal aggression in eNOS-/- mice was examined and found to be normal relative to wild-type (WT) mice in terms of the percentage displaying aggression, the average number of attacks against a male intruder, and the total amount of time spent attacking the male intruder. The eNOS-/- females also displayed normal pup retrieval behavior. Because a significant elevation of citrulline, an indirect marker of NO synthesis, occurs in neurons of the hypothalamus of lactating WT mice in association with maternal aggression, we examined the brains of eNOS-/- females for citrulline immunoreactivity following an aggressive encounter. The aggressive eNOS-/- females exhibited a significant elevation of citrulline in the medial preoptic nucleus and the subparaventricular zone of the hypothalamus relative to unstimulated lactating eNOS-/- females. Taken together, these results suggest that NO produced by eNOS neither facilitates nor inhibits maternal aggression and that NO produced by eNOS has a different role in maternal and male aggression.     

Extra-pair copulations,intra-specific brood parasitism,and quasi-parasitism in birds: a theoretical approach

Although 90 % of all bird species are monogamous, many species practice alternative reproductive strategies as extra-pair copulations, intra-specific brood parasitism, and quasi-parasitism. In territorial monogamous species, both partners hold and defend the territory from intruders. Often, the intruders are males and usually the local male banishes the intruders. Indeed, many studies focused on the response of the local male toward intruder males. However, the benefits and costs associated with the responses of the local male toward intruder females have been largely overlooked. Focusing mainly on alternative reproductive strategies, we developed a model to predict the aggression a monogamous male may demonstrate toward an intruder female during the pre-egg laying stage of his local female partner. This model demonstrates that the intensity of aggression that the local male shows toward an intruder female depends on the extra-pair copulations that his local female partner may perform. Further, the aggression also depends upon intra-specific brood parasitism and quasi-parasitism that might be carried out by the intruder female. Our approach suggests that when considering mating strategies, there is a need to assess how these three alternative reproductive strategies may affect the local male's aggression toward intruder females.     

Male and female cooperatively breeding fish provide support for the "Challenge Hypothesis"

The idea that territorial aggression is regulated by androgensand that aggression itself can modulate androgen levels is wellestablished in males. In many species, females also displayaggressive behavior, yet little work has been conducted on theeffects of female aggression on hormone levels. In this study,we compared the effects of a simulated territory intrusion (amethod for testing the Challenge Hypothesis) on males and femalesof the fish, Neolamprologus pulcher. This cichlid fish fromLake Tanganyika is a particularly useful species to examinesex differences in the behavioral mediation of hormones as breedingpairs remain in a territory year round and both sexes defendthis territory against conspecific and heterospecific intruders.In our study, both sexes indeed aggressively defended theirterritory against a simulated territory intruder. In responseto intruders, both males and females displayed elevated levelsof circulating 11-ketotestosterone, but only females exhibitedincreases in testosterone. Neither aggressing male nor femalefish showed changes in estradiol levels compared to control(nonaggressing) fish. Residents were more aggressive than theintruders and won most of the interactions. However, residents(or winners) did not show higher hormone levels than intruders(or losers). We suggest that aggression commonly modulates androgenlevels in both male and female teleost fish.     

Resource attractiveness of the male beaugregory damselfish and his decision to court or defend

We examined the decisions territorial male beaugregory damselfish (Stegastes leucostictus) make when presented with mating and aggressive situations simultaneously. Specifically, we testedhow males responded to simultaneous and consecutive presentationsof conspecific males and females in bottles. We hypothesizedthat (1) territorial males would show lower levels of courtshiptoward females when a competing male is also present comparedto when only the female is present and (2) territorial maleswould show higher levels of aggression toward intruding maleswhen a female is also present on their territories than whenonly the intruder is present. We predicted that males withhigh-quality breeding sites would court females and attackcompetitors more vigorously than males with low-quality breedingsites. Males on low-quality breeding sites exhibited fewerconspicuous courtship displays toward bottled females and alower bite rate toward bottled males than did the males onhigh-quality breeding sites. We concluded that poor breeding-sitequality was responsible for the decline in the most conspicuous aspects of both courtship and aggression. When presented simultaneouslywith a bottled male and a bottled female, defenders of bothbreeding-site types drastically reduced the number of courtshipdisplays and the amount of time they spent near the female.Thus, all aspects of courtship were reduced in the presenceof a male intruder. Time spent near the bottled male also decreased in these simultaneous presentations; however, this decreasewas less dramatic than the reduction in time spent near bottledfemales. Habitat quality did not affect these trade-off decisions,but the bite rate exhibited toward the bottled male increasedin the simultaneous presentations compared to the single presentations.Due to this increase in a territorial male's defensive behaviorwhen a female is present, we conclude that the presence of afemale temporarily increased the value of a territory. We suggestthat the possible loss of a territory to an intruding maletakes priority over the potential benefits of successfullycourting a single female and that it is a male's future reproduction,as well as his current reproduction, by which he assesses hisbenefits.     

Effect of paired encounters on plasma androgens and behaviour in males and females of the spiny damselfish Acanthochromis polyacanthus

Sexually mature male and female spiny damselfish, Acanthochromis polyacanthus (Pomacentridae) were introduced to resident fish of both sexes in paired encounter trials and the effect on activity, agonistic behaviour and plasma levels of testosterone (T) and 11-ketotestosterone (11-KT) in males, and T and 17β-estradiol (E₂) in females, and cortisol in both sexes was determined. Introduced males showed suppressed levels of T in the presence of both resident males and females, whereas resident males showed elevated T in response to introduced males but not females. Plasma 11-KT levels were unchanged in either resident or introduced males. Resident males showed increased activity in the presence of males but not females. Resident females showed an increase in activity when paired with introduced females and greater aggressive behaviour towards females than males. There were no differences in plasma hormone levels in either resident or introduced female fish. Plasma cortisol levels were low in all fish and stress effects did not appear to account for differences in T levels in males. The results of the present study show that elevations in plasma T levels in resident male spiny damselfish are associated only with male presence but that suppression of T in introduced fish occurs irrespective of the sex of the resident. In contrast resident females, which show stronger evidence of aggressive behaviour do not show changes in plasma androgen levels. This suggests that aggressive behaviour in male and female fishes may be mediated by different endocrine pathways.     

Non-migratory stonechats show seasonal changes in the hormonal regulation of non-seasonal territorial aggression

In many birds and mammals, male territorial aggression is modulated by elevated circulating concentrations of the steroid hormone testosterone (T) during the breeding season. However, many species are territorial also during the non-breeding season, when plasma T levels are basal. The endocrine control of non-breeding territorial aggression differs considerably between species, and previous studies on wintering birds suggest differences between migratory and resident species. We investigated the endocrine modulation of territorial aggression during the breeding and non-breeding season in a resident population of European stonechats (Saxicola torquata rubicola). We recorded the aggressive response to a simulated territorial intrusion in spring and winter. Then, we compared the territorial aggression between seasons and in an experiment in which we blocked the androgenic and estrogenic action of T. We found no difference in the aggressive response between the breeding and the non-breeding season. However, similarly to what is found in migratory stonechats, the hormonal treatment decreased aggressive behaviors in resident males in the breeding season, whereas no effects were recorded in the non-breeding season. When we compared the aggressive responses of untreated birds with those obtained from migratory populations in a previous study, we found that territorial aggression of resident males was lower than that of migratory males during the breeding season. Our results show that in a resident population of stonechats T and/or its metabolites control territorial aggression in the breeding but not in the non-breeding season. In addition, our study supports the hypothesis that migratory status does modulate the intensity of aggressive behavior.     

Resource defense and juvenile hormone: the "challenge hypothesis" extended to insects

As predicted for vertebrates by the challenge hypothesis, the endocrine system of invertebrates can respond to social stimuli to modulate aggression. Testosterone (T) is generally considered to moderate aggression associated with reproduction, i.e. the establishment of breeding territories, mate guarding and offspring defense; juvenile hormone (JH) serves an analogous function in burying beetles. Hemolymph titers of JH increase significantly in Nicrophorus orbicollis, a species with facultative biparental care, when challenged by an intruder to defend their resource. During the first 12 h after the discovery of a carcass, the necessary breeding resource, competition is intrasexual, and JH of males responds only to a challenge by males, and JH of females responds only to a challenge by female intruders. After this period, competition is intersexual, and JH increases significantly in both males and females challenged by an intruder of either sex. In contrast, JH titers in a nonparental species are much higher throughout the breeding season, and neither males nor females respond hormonally to an intruder. These findings support the challenge hypothesis and suggest that mating systems and breeding strategies can promote plastic responses in insect, as well as vertebrate, endocrine systems.     

The Costs of Confronting Infanticidal Intruders in a Burying Beetle

Infanticide by unrelated adults is a complex behavior in burying beetles (Nicrophorus spp.) serving multiple functions (resource competition, access to mates, cannibalism). The costs of confronting an infanticidal intruder are likely to vary with context. To assess these costs for a single female parent (Nicrophorus pustulatus), we systematically manipulated the sex of a conspecific intruder and the timing of the intrusion. Male intruders were a greater takeover threat than female intruders, and infanticidal takeovers were more common earlier in the breeding cycle. Even though a male intruder posed a greater threat to the brood, a female intruder was a greater threat to the reproductive success of the resident female. Female intruders that took over a carcass excluded the resident female from the resource. When a male intruder took over a carcass, the resident female was able to recover much of her loss by producing a replacement brood. Even when females successfully defended their broods, they suffered decreased reproductive output relative to control females that never had to confront an intruder (expt 1), but the mechanisms underlying this cost were unclear. To test the hypothesis that defeated female intruders attempt to parasitize late‐stage broods, female intruders whose eggs could be identified by a fat‐soluble dye were introduced to resident females caring for larvae (expt 2). Fifteen of 20 intruders oviposited eggs and the number of eggs were related to intrusion pressure. Because resident females rarely produced eggs while caring for larvae, it is uncertain whether the behavior of the defeated female should be characterized as brood parasitism, a failed takeover attempt, or an attempt to use the remains of the depleted resource. This study provides the most complete picture of the changing costs of confronting an infanticidal threat throughout the vulnerable period of offspring development.     

Female Intrasexual Territoriality and its Potential Adaptive Significance: The Pampean Grassland Mouse as an Ecological Model Species

Territorial behaviour in female small mammals has been proposed as a mechanism to defend limited ecological resources or their pups against conspecific infanticidal or predators. Female territorial behaviour very often is associated with reproductive activity due to the fact that frequency and intensity of aggression are exhibited mainly when females are pregnant or lactating. In vole and mice species, female territoriality would be a counterstrategy to prevent the killing of their pups by conspecific breeding females. To study whether female territoriality is a strategy for pups or nest defence against infanticidal breeding females, and whether time invested in nursing young affects aggressive response of mothers, we used the Pampean grassland mouse (Akodon azarae) as an ecological model species. We conducted resident–intruder tests between lactating females. Differences in residency time (48 vs. 72 h) of focal females in their home territory were also included in the analysis. In all cases, the pups of both resident and intruder mothers were placed with the nesting material from their reproductive cages. Resident mothers were always more aggressive than intruders and they were even more aggressive when they spent more time nursing their pups. Contrarily, intruder females exhibited the greatest values of submissive behaviours. Our results show that female territoriality of A. azarae would represent a strategy to protect pups from potentially infanticidal females. We discuss the extent of female intrasexual territoriality and its potential adaptive significance in relation to strategies which lead to increase their reproductive success.     

Ovarian Hormones Influence Territorial Aggression in Free-Living Female Mountain Spiny Lizards

Females are aggressive in many species but relatively little is known about the hormonal basis of female aggression, especially in free-living animals. Female mountain spiny lizards aggressively defend territories from other females. Previously, we showed that plasma levels of testosterone (T) and estradiol (E) are positively associated with levels of female aggression. Here, we manipulated hormone levels in free-living females and examined aggression expressed by females returned to their natural territories. Females received one of the following: (1) ovariectomy + empty implant (OVEX), (2) ovariectomy + T implant (T-IMP), or (3) sham surgery + empty implant (SHAM). OVEX females had reduced plasma levels of E but not T relative to SHAM females. T-IMP females had elevated plasma levels of T. Levels of display and aggression in OVEX females were reduced relative to SHAM females. T-IMP females had restored levels of display behavior although, unlike SHAM, no T-IMP females expressed the overt aggressive behavior of charging. These data are most consistent with the hypothesis that an ovarian factor such as E promotes female aggression, since ovariectomy reduced both plasma E and aggression but had no effect on plasma T. The results from the T-IMP females are also consistent with this hypothesis if we assume that the effects of T are due to aromatization to E in target tissues. The data do not rule out a role for T in promoting female aggression since T-implants resulted in elevated plasma T and restored display behaviors. This study represents one of the first studies examining the hormonal basis of female aggression in free-living females.     

Winning fights elevates testosterone levels in California mice and enhances future ability to win fights

The 'winner effect' has been studied in a variety of species, but only rarely in mammals. We compared effects of winning three, two, one, or zero resident-intruder encounters on the likelihood of winning a subsequent aggressive encounter in the California mouse (Peromyscus californicus). During the training phase, we ensured that resident males won all encounters by staging contests with mildly sedated, smaller intruders. During the test phase, the resident male encountered an unfamiliar, more evenly matched intruder that had experience winning an encounter and was larger than the resident. Testosterone (T) plasma levels significantly increased after the final test when they had experienced two prior winning encounters, and the probability of winning a future encounter increased significantly after three prior wins independent of intrinsic fighting ability. We hypothesize a 'winner-challenge' effect in which increased T levels serve to reinforce the winner effect in male California mice.     

Progesterone modulates aggression in sex-role reversed female African black coucals

Testosterone is assumed to be the key hormone related to resource-defence aggression. While this role has been confirmed mostly in the context of reproduction in male vertebrates, the effect of testosterone on the expression of resource-defence aggression in female vertebrates is not so well established. Furthermore, laboratory work suggests that progesterone inhibits aggressive behaviour in females. In this study, we investigated the hormonal changes underlying territorial aggression in free-living female African black coucals, Centropus grillii (Aves; Cuculidae). Females of this sex-role reversed polyandrous bird species should be particularly prone to be affected by testosterone because they aggressively defend territories similar to males of other species. We show, however, that territorial aggression in female black coucals is modulated by progesterone. After aggressive territorial challenges female black coucals expressed lower levels of progesterone than unchallenged territorial females and females without territories, suggesting that progesterone may suppress territorial aggression and is downregulated during aggressive encounters. Indeed, females treated with physiological concentrations of progesterone were less aggressive than females with placebo implants. This is one of the first demonstrations of a corresponding hormone-behaviour interaction under challenged and experimental conditions in free-living females. We anticipate that our observation in a sex-role reversed species may provide a more general mechanism, by which progesterone--in interaction with testosterone--may regulate resource-defence aggression in female vertebrates.     

Immigration in wild groups of golden lion tamarins (Leontopithecus rosalia)

Seventeen territorial groups of wild golden lion tamarins were monitored for periods of 10–76 months. Immigration into established groups was rare (0.48 immigrating individuals per group per year) and occurred mostly in the context of replacement of breeding individuals. Nonreplacement immigration events usually occurred in conjunction with some other change in group composition (e.g., an emigration or another immigration). Aggression by resident tamarins toward potential immigrants appeared to be the proximate factor limiting movement into groups. Most such aggression was intrasexual, but potential female immigrants were sometimes chased by male as well as female residents. Immigration was highly male biased (85% of individuals). Factors possibly contributing to this bias were inheritance of breeding positions by adult daughters (reducing female and increasing male immigration opportunities), ability of males but not females to join groups already containing a same-sex breeding individual, and the fact that potential female immigrants appeared to face some intersexual as well as intrasexual aggression. Male and female roles in the maintenance of a monogynous mating system are considered in light of these results. Contrasts with data from intruder studies on captive golden lion tamarins [French & Inglett, Animal Behaviour 37:487–497, 1989] are discussed. © 1996 Wiley-Liss, Inc.     

Effects of resource distribution on activity and territory defence in house mice, Mus domesticus

How much an animal invests in defending a territory depends, in part, on the quality, quantity and distribution of resources, but do animals target their investment in defence within the territory according to the location of different resources? We examined whether wild-caught male and female house mice increased aggression towards intruders of the same or opposite sex when in areas containing their food/water or nest site. Pairs of resident mice were established in enclosures consisting of two areas. In split enclosures, food and water were in one area and a nest site in the other, while in clumped enclosures all resources were in one area with no resources in the other. Residents of both sexes were quicker to attack intruders, and were more aggressive, in areas containing resources than in an area containing no resources. There was no difference in aggression between areas containing food/water, a nest site or both. The effect of resources on territorial defence was due largely to changes in aggression against intruders of the opposite sex. Residents, especially males, attacked intruders of their own sex more than those of the opposite sex. This bias was much stronger when no resources were present, owing to low aggression against opposite-sex intruders in the absence of resources. There were no differences in intruder aggression, and the relative size of the intruder (heavier or lighter than the resident) had no effect on resident aggression. Residents also spent less time out of their nest in clumped enclosures owing to low activity in the nonresource area.