Spring and autumn territoriality in song sparrows: same behavior, different mechanisms?

Vertebrates show a diverse array of social behaviors associatedwith territoriality. Field and laboratory experiments indicatethat underlying themes—including mechanisms—mayexist. For example in birds, extensive evidence over many decadeshas implicated a role for testosterone in the activation ofterritorial aggression in reproductive contexts. Territorialityat other times of the year appeared to be independent of gonadalhormone control. One obvious question is—why this diversityof control mechanisms for an apparently similar behavior? Controlof testosterone secretion during the breeding season must balancethe need to compete with other males (that tends to increasetestosterone secretion), and the need to provide parental care(that requires lower testosterone concentrations). Regulationof aggressive behaviors by testosterone in the non-breedingseason may incur substantial costs. A series of experimentson the male song sparrow, Melospiza melodia morphna, of westernWashington State have revealed possible mechanisms to avoidthese costs. Song sparrows are sedentary and defend territoriesin both breeding and non-breeding seasons. Dominance interactions,territorial aggression and song during the non-breeding seasonare essentially identical to those during the breeding season.Although in the non-breeding season plasma testosterone andestradiol levels are very low, treatment with an aromatase inhibitordecreases aggression and simultaneous implantation of estradiolrestores territorial behavior. These data suggest that the mechanismby which testosterone regulates territorial behavior at theneural level remains intact throughout the year. How the hormonalmessage to activate such behavior gets to the brain in differentseason does, however, appear to be different.     

Neurobiological correlates premeditated (learned) aggression: seeking new experimental approaches]

Theoretical possibility of experimental modeling of learned (premediated) aggression developing in human after experience of aggression is considered. The sensory contact technique increases aggressiveness in male mice and allows aggressive type of behavior to be formed as a result of repeated experience of victories in daily agonistic confrontations. Some behavioral domains confirm the development of learned aggression in males similar to those in humans. The features are: repeated experience of aggression reinforced by victories; elements of learned behavior after period of confrontations; intent, measured by increase of the aggressive motivation prior agonistic confrontation; decreased emotionality estimated by parameters of open field behavior. Relevant stimuli provoke demonstration of aggression. This review summarized data on the influence of positive fighting experience in daily intermale confrontations on the behavior, neurochemistry and physiology of aggressive mice (winners). This sort of experience changes many characteristics in individual and social behaviors, these having been estimated in different tests and in varied situations. Some physiological parameters are also changed in the winners. Neurochemical data confirm the activation of brain dopaminergic systems and functional inhibition of serotonergic system in winners under influence of repeated experience of aggression. The expression of the neurochemical and behavioral changes observed in winners has been found dependent on the mouse strain and on the duration of their agonistic confrontations. Similarities in mechanisms of learned aggression in humans and mice are considered.     

A method for quantifying aggression in male Drosophila melanogaster

Aggressive behavior is a complex social behavior that is difficult to measure. Here, we describe a simple method for the quantitative analysis of aggression in male Drosophila melanogaster. Traditional measurements of aggressive behavior have relied on a territorial context with a food territory and a female as factors that induce or enhance aggression. The protocol described here is devoid of a food territory or a female, making it simpler than most existing methods used to measure aggressive behavior. Multiple pairs of males are tested simultaneously to obtain an average fighting score. Four parameters are used to quantify the behavior: frequency, index, latency and intensity of fighting based on unambiguous offensive fighting behaviors. The assay takes 15 min, during which time a frequency score is obtained for 20-35 pairs simultaneously. More in-depth analysis, including latency, index and intensity, can be performed on the videotaped record of the experiment. The assay is highly reproducible and requires limited resources in a simple setup.     

Intra- and interspecific social and aggressive behaviour in the Siamese fighting fish, Betta splendens

Siamese fighting fish and paradise fish were operantly conditioned to swim through a cylinder to open a door allowing them to explore visually conspecifics, non-conspecifics, or inanimate objects. All stimuli significantly elevated response levels compared to control conditions, but response rate for conspecifics was not higher than for other stimuli. In experiments 2 and 3, fighting fish threatened and attacked non-conspecifics as well as conspecifics, and using a blind procedure, displays to different fish could not be easily differentiated. A final experiment with models failed to reveal any specific shape critical to the elicitation of the threat display. Discussion considers the possibility that the operant behaviour of the fighting fish may be motivated by visual exploration as well as by aggression, and that in actual fighting the social behaviour of the opponent may be more crucial than any particular visual stimulus.     

Effects of physical and social experiences and octopamine receptor agonist on fighting behavior of male crickets Velarifictorus aspersus (Orthoptera: Gryllidae)

Fighting commonly occurs among animals and is very important for resolving conflicts between conspecific individuals over limited resources. The plasticity of fighting strategies and neurobiological mechanisms underlying fighting behavior of insects are not fully understood. In the present study, we examined whether physical and social experiences affected the aggressiveness of males of the cricket Velarifictorus aspersus Walker, and whether an octopamine (OA) receptor agonist could affected the aggressiveness of males exposed to different experiences. We found that flight and winning a fight significantly enhanced male aggressiveness, while losing a fight significantly suppressed male aggressiveness, consistent with the findings of existing studies on other cricket species. We also found that female presence had a stronger enhancing effect on male aggressiveness than flight or winning a fight. These findings demonstrated that physical and social experiences can affect the fighting behavior of male V. aspersus. Topical application of a 0.15?M solution of an OA receptor agonist (chlordimeform, CDM) significantly increased male aggression level, suggesting that OA may play an important role as a neuromodulator in controlling fighting behavior of males of this species. Despite displaying a significantly higher aggression level (level 5 or 6), CDM-treated losers did not escalate to physical combat, while fights between courting males usually resulted in physical escalation. It is likely that fighting behavior is only partly regulated by OA, and additional regulatory pathways may be involved in achieving physical combat.     

Intraspecific competition influences the symmetry and intensity of aggression in the Argentine ant

Cooperative social groups rely on the ability to distinguishmembers from nonmembers. Accordingly, social insects have evolveda variety of systems that allow discrimination of nest matesfrom non–nest mates. In this study, we show that experiencecan modify patterns of intraspecific aggression in Argentineants (Linepithema humile). In laboratory experiments, we foundthat aggression between colonies was often asymmetrical, butin all five cases, this asymmetry shifted to symmetrical aggressionafter contact with a hostile colony. Moreover, in the field,aggression between workers collected from colony borders wassymmetrical, whereas polarized aggression occurred between workerscollected 500 m away from colony borders. Coinciding with thisshift in aggression symmetry, we also observed an increase inboth the overall level of aggression and the frequency of aggressionin both the field and laboratory bioassays. We found littleevidence for colony-level competitive asymmetries stemming frompolarities in aggression at the worker level, either in thelaboratory or in the field. These results illustrate that recognitionsystems in Argentine ants are surprisingly dynamic and provideexperimental evidence for how recognition can be adjusted inresponse to specific circumstances—in this case the presenceof intraspecific competitors.     

Intragroup agonistic behavior in captive groups of the common marmosetCallithrix jacchus jacchus

Agonistic behavior was observed in five captive groups of the monogamous monkey Callithrix jacchus jacchus,which normally produces twin offspring every 5 months. Fighting is first recorded when twins are aged 5–10 months. These “twin fights” determine differences in status between combatants that can be detected 5 months later. From what is known of the social behavior of the species, it is postulated that an individual’s twin is its most serious rival and that early fighting is advantageous because injury is minimal while the animal retains its milk dentition. In contrast to twin fights, aggression between same-sex juveniles and adults does not involve long fights and probably serves to reinforce preexisting differences in status. It often results in forcing a group member to the periphery, and therefore, its main function may be to drive mature, same-sexed individuals out of the group. Apart from the relationship between twins, status within the family group is age related and not normally determined by aggression.     

Stress and the development of agonistic behavior in golden hamsters

Aggressive behavior can be studied as either offensive or defensive responses to a stimulus. The studies discussed in this review are focused on the peripubertal development of offensive aggression in male golden hamsters and its responsiveness to repeated social stress. Quantitative and qualitative changes in offensive responses were analyzed during this period. Quantitative changes in offensive responses were observed as decreased frequency of attacks. Qualitative changes were observed as changes in attack types, as animals reorient their attacks gradually from the face to the lower belly and rump. These developmental changes were altered by repeated exposure to social stress during early puberty. Daily exposure to aggressive adults during early puberty accelerated the qualitative development of offensive responses and the onset of adult-like offensive responses. In contrast, social stress had little effect on the quantitative changes associated with early puberty. However, social stress was associated with higher attack frequency during adulthood. These effects of stress during early puberty contrast with those observed with animals in late puberty. At that time, repeated exposure to aggressive adults inhibits offensive aggression. These data constitute the basis for a new theory on the development of agonistic behavior that includes the following hypotheses. First, it is hypothesized that mid-puberty is marked by a change in responsiveness to repeated social stress. As such, differences in stress responsiveness from social interactions are interpreted as a basic distinction between play fighting and adult aggression. Second, it is also hypothesized that a common neural circuitry mediates the activation of offensive responses during play fighting and adult aggressive interactions.     

Male Siamese Fighting Fish, Betta splendens, Increase Rather than Conceal Courtship Behavior when a Rival is Present

The impact of social environment on mating success is especially pronounced in species where both intraspecific and interspecific selection influence reproduction, such as the Siamese fighting fish. Males alter male–male interactions when either a male or female audience is present, but how males change their behavior toward a female when a rival male is present is unknown. This study addresses whether males alter their behavior toward a female in a way that would prevent a rival male from interrupting courtship. The behavior of male Siamese fighting fish toward a dummy female was examined under various degrees of visual cover, both in the presence and absence of a rival male, to investigate whether males use concealment provided by the structural environment to their advantage. While males did not use barriers to conceal courtship as hypothesized, males altered their behavior by increasing courtship and monitoring their nest when a rival was visible. This increase in courtship is in contrast to most studies on courtship in the presence of a rival that find a reduction in courtship behavior. Males spent more time opercular gill flaring when no barriers were present, suggesting that males may be trying to court the female and communicate to the rival simultaneously. There was also a trend for aggression toward the female and the rival to decrease as screen length increased. Thus, males compensate for the presence of a rival by adjusting their courtship and aggressive behaviors, which could have important implications for courtship success.     

The Ontogeny of Play within a Society: Preliminary Analysis

Data were collected on play behaviors occuring within a singletroop or rhesus monkeys in two environments. Observations wereregular and covered a total of almost 2 years. The three categoriesof play—object, activity, and social play—tendedto occur together, typically within the same recording session.Thus, the attending conditions—including satiation andmaturity—which permitted the occurrence of one categoryof play behavior, permitted the occurrence of the other categoriesas well. Maturity seemed to account for the appearance of aparticular behavior within a category (e.g., manipulation ratherthan touching; climbing rather than active hanging; rompingand wrestling rather than contact or touching). The social context,determined by such factors as maternal dominance, the identityof nearby animals, and the overall social tension of the troop,and reflected in the extent of inhibitory control of the targetanimals by their mothers, seemed to determine the frequencywith which these elements in the infant monkey's repertoirecould be displayed during any given period in the ontogeny ofthe individual.     

Rats Benefit from Winner and Loser Effects

Prior fighting experience of opponents can influence the outcome of conflicts. After a victory, animals are more likely to win subsequent contests, whereas after a defeat animals are more likely to lose, regardless of the identity of opponents. The underlying mechanisms and the adaptive significance of these winner and loser effects are as yet unknown. Here, we tested experimentally whether agonistic behavior of male wild‐type Norway rats is influenced by social experience, and we investigated whether this might reduce fighting costs (duration of contest, risk of injury) in subsequent encounters. Rats were randomly assigned to receive either a losing or a winning experience and subsequently tested with unfamiliar, naïve opponents. We found that most rats with a winning experience won the subsequent encounter, and all rats with a losing experience lost the next contest. Previous winners attacked more rapidly in the subsequent encounter and reduced their aggressive behavior sooner; the contests were decided more quickly, which saved time and behavioral effort to the winner. Previous losers received less aggression in the next encounter, despite emitting fewer submissive ultrasonic calls than in the preceding contest, thereby reducing the risk of being injured by the opponent. Thus, anonymous social experience influenced rats’ subsequent behavior toward size‐matched, naïve, unknown social partners. Furthermore, apparently, they benefit from showing winner and loser effects in intraspecific contests by saving time, energy, and risk.     

Studying aggression in Drosophila (fruit flies)

Aggression is an innate behavior that evolved in the framework of defending or obtaining resources. This complex social behavior is influenced by genetic, hormonal and environmental factors. In many organisms, aggression is critical to survival but controlling and suppressing aggression in distinct contexts also has become increasingly important. In recent years, invertebrates have become increasingly useful as model systems for investigating the genetic and systems biological basis of complex social behavior. This is in part due to the diverse repertoire of behaviors exhibited by these organisms. In the accompanying video, we outline a method for analyzing aggression in Drosophila whose design encompasses important eco-ethological constraints. Details include steps for: making a fighting chamber; isolating and painting flies; adding flies to the fight chamber; and video taping fights. This approach is currently being used to identify candidate genes important in aggression and in elaborating the neuronal circuitry that underlies the output of aggression and other social behaviors.     

Embryonic Pituitary Adrenal Axis, Behavior Development and Domestication in Birds

ACTH and corticosterone exert opposite effects on the approachand imprinting behavior of newly hatched ducklings. Wild mallardand domesticated Pekin ducklings differ in the early posthatchperiod in both plasma corticosterone levels and approach/avoidancebehaviors. Injection of Pekin duckling embryos with pituitary—adrenocorticalhormones alters both later adrenal function and certain aspectsof posthatch behavior. These birds have behavioral and hormonalcharacteristics which resemble those of wild mallards. The hypothesisthat behavioral differences in wild and domesticated ducklingsresult from a higher level of pituitary adrenal function inthe wild embryo is explored. Although adrenocortical functionchanges during domestication in many species, evidence thatthe hormonal changes mediate the concomitant changes in approachand avoidance behavior remains inconclusive. Factors which causeadrenal function and early behaviors to differ in wild and domesticatedgenotypes must be sought in the gene action during embryonicdevelopment. Since imprinting behavior is modulated by pituitary—adrenalhormones, any factor which affects post—hatch adrenalfunction may potentially affect imprinting. Later behavior developmentin the adult is strongly dependent on neonatal experiences;and, therefore, hormonal modulation of early imprinting behaviormay constitute an important determinant of adult social behavior.     

Repeated exposure to social stress alters the development of agonistic behavior in male golden hamsters

In male golden hamsters, exposure to social stress during puberty alters aggressive behavior. Interestingly, agonistic behavior undergoes two major transitions during puberty: a decline in attack frequency and a shift from play fighting to adult-like aggression. Based on previous observations, we developed an approach for characterizing offensive responses as play fighting or adult-like. The present studies had two aims. First, we validated our approach by looking at the development of attack types during puberty. Second, we looked at the effects of repeated social stress on the development of agonistic behavior by repeatedly exposing individuals to aggressive adults during puberty. In the first phase of the study, our results point to three different developmental periods. Initially, animals engage in agonistic behavior though attacks targeted at the face and cheeks. This period lasts from Postnatal Day 20 (P-20) to P-40 (early puberty). This phase corresponding to play fighting is followed by a transitional period characterized by attacks focused on the flanks (from P-40 to P-50, mid-puberty). Afterward, animals perform adult-like aggression characterized by attacks focused on the belly and rear. Our data also show that repeated exposure to aggressive adults has two separate effects on the development of agonistic behavior. Repeated social stress accelerated the onset of adult-like agonistic responses. Furthermore, attack frequency, while decreasing during puberty, remained at a higher level in early adulthood in stressed animals. These results show that repeated exposure to social stress during puberty alters the development of agonistic behavior both qualitatively and quantitatively.     

Expectation modulates neural responses to pleasant and aversive stimuli in primate amygdala

Animals and humans learn to approach and acquire pleasant stimuli and to avoid or defend against aversive ones. However, both pleasant and aversive stimuli can elicit arousal and attention, and their salience or intensity increases when they occur by surprise. Thus, adaptive behavior may require that neural circuits compute both stimulus valence--or value--and intensity. To explore how these computations may be implemented, we examined neural responses in the primate amygdala to unexpected reinforcement during learning. Many amygdala neurons responded differently to reinforcement depending upon whether or not it was expected. In some neurons, this modulation occurred only for rewards or aversive stimuli, but not both. In other neurons, expectation similarly modulated responses to both rewards and punishments. These different neuronal populations may subserve two sorts of processes mediated by the amygdala: those activated by surprising reinforcements of both valences-such as enhanced arousal and attention-and those that are valence-specific, such as fear or reward-seeking behavior.     

Evolutionary Perspectives on Human Aggression

The papers in this volume present varying approaches to human aggression, each from an evolutionary perspective. The evolutionary studies of aggression collected here all pursue aspects of patterns of response to environmental circumstances and consider explicitly how those circumstances shape the costs and benefits of behaving aggressively. All the authors understand various aspects of aggression as evolved adaptations but none believe that this implies we are doomed to continued violence, but rather that variation in aggression has evolutionary roots. These papers reveal several similarities between human and nonhuman aggression, including our response to physical strength as an indicator of fighting ability, testosterone response to competition, a sensitivity to paternity, and baseline features of intergroup aggression in foragers and chimps. There is also one paper tackling the phylogeny of these traits. The many differences between human and nonhuman aggression are also pursued here. Topics here include the impact of modern weapons and extremes of wealth and power on both the costs and benefits of fighting, and the scale to which coercion can promote aggression that acts against a fighter’s own interests. Also the implications of large-scale human sociality are discussed.     

Effects of social isolation on aggressiveness in fish with special reference to the swordtail (Xiphophorus helleri)

The attack readiness of socially isolated male swordtails ($\text{Xiphophorus helleri}$) was measured in two different aggression tests: (a) In the standard–opponent test the aggressive responses to a small, rather passive opponent swimming in a small adjacent compartment of the test aquarium were counted. (b) In the mirror test the subjects were confronted with their own mirror image. Social isolation for 4 weeks resulted in a decrease of attack readiness in both test situations. It is concluded that -- similar to cichlids -- external stimuli from conspecifics are essential for maintaining the level of aggression readiness characteristic for socially living males. There are good reasons to propose that the effect of external stimuli is mediated by the pituitary-gonadal axis. On the other hand, it is well known from previous studies that, in escalated encounters between freely swimming males, isolated males fight longer and at higher intensities for rank-order position than non-isolated males. The hypothesis is proposed that the high fighting intensity of previously isolated males could be due to an experience levelling effect of social isolation, i.e. the influence of different agonistic experience is reduced by isolation.A critical review of the literature on isolation-induced decremental and incremental effects on aggression in teleosts is presented. Often it is extremely difficult to compare the results of different authors because the methods of behavioural measurement differ to a large extent. However, it is a striking fact that social isolation of immature fish in all known cases has resulted in an increase of aggressiveness. Probably in mature males, depending on species and circumstances, either an incremental or a decremental effect of social isolation may be adaptive. On the one hand, a spontaneous increase of attack readiness may be advantageous for defence of a territory or a position in the social hierarchy and improves the ability of a single individual to join a group of strange conspecifics. On the other hand, it may be economic to lower the level of androgenic hormones to some extent in the absence of conspecifics, and this could lead to a reduction of the aggression level.     

Dynamics and mechanics of social rank reversal

Stable social relationships are rearranged over time as resources such as favored territorial positions change. We test the hypotheses that social rank relationships are relatively stable, and although social signals influence aggression and rank, they are not as important as memory of an opponent. In addition, we hypothesize that eyespots, aggression and corticosterone influence serotonin and N-methyl-D-aspartate (NMDA) systems in limbic structures involved in learning and memory. In stable adult dominant-subordinate relationships in the lizard Anolis carolinensis, social rank can be reversed by pharmacological elevation of limbic serotonergic activity. Any pair of specific experiences: behaving aggressively, viewing aggression or perceiving sign stimuli indicative of dominant rank also elevate serotonergic activity. Differences in the extent of serotonergic activation may be a discriminating and consolidating factor in attaining superior rank. For instance, socially aggressive encounters lead to increases in plasma corticosterone that stimulate both serotonergic activity and expression of the NMDA receptor subunit 2B (NR_2B) within the CA₃ region of the lizard hippocampus. Integration of these systems will regulate opponent recognition and memory, motivation to attack or retreat, and behavioral and physiological reactions to stressful social interactions. Contextually appropriate social responses provide a modifiable basis for coping with the flexibility of social relationships.     

Role of the olfactory pathway in agonistic behavior of crayfish, <Emphasis Type="Italic">Procambarus clarkii</Emphasis>

Crayfish establish social dominance hierarchies through agonistic interactions, and these hierarchies are maintained through assessment of social status. Chemical signals influence several aspects of fighting behavior, but the specific chemosensory sensilla involved in detecting these signals in crayfish are unknown. The goal of our study was to examine the importance of aesthetasc sensilla—olfactory sensors on the antennules of decapod crustaceans—in regulating changes in fighting behavior in crayfish, Procambarus clarkii, over the course of repeated pairings. We selectively ablated aesthetascs from pairs of crayfish after the first day of trials and compared the behavior of these ablated animals to that of pairs of intact controls. Results show that unablated crayfish significantly decreased the number and duration of fights over repeated pairings, whereas crayfish lacking aesthetascs continued to engage in similar amounts of fighting across all three trial days. This difference shows that aesthetascs regulate fighting behavior in P. clarkii.     

Fighting while Parasitized: Can Nematode Infections Affect the Outcome of Staged Combat in Beetles?

The effects of non-lethal parasites may be felt most strongly when hosts engage in intense, energy-demanding behaviors. One such behavior is fighting with conspecifics, which is common among territorial animals, including many beetle species. We examined the effects of parasites on the fighting ability of a saproxylic beetle, the horned passalus (Odontotaenius disjunctus, Family: Passalidae), which is host to a non-lethal nematode, Chondronema passali. We pitted pairs of randomly-chosen (but equally-weighted) beetles against each other in a small arena and determined the winner and aggression level of fights. Then we examined beetles for the presence, and severity of nematode infections. There was a non-significant tendency (p = 0.065) for the frequency of wins, losses and draws to differ between beetles with and without C. passali; non-parasitized individuals (n = 104) won 47% of their fights while those with the parasite (n = 88) won 34%, a 13% difference in wins. The number of nematodes in a beetle affected the outcome of fights between infected and uninfected individuals in an unexpected fashion: fighting ability was lowest in beetles with the lowest (p = 0.033), not highest (p = 0.266), nematode burdens. Within-fight aggression was highest when both beetles were uninfected and lowest when both were infected (p = 0.034). Collectively, these results suggest the nematode parasite, C. passali, is associated with a modest reduction in fighting ability in horned passalus beetles, consistent with the idea that parasitized beetles have lower energy available for fighting. This study adds to a small but growing body of evidence showing how parasites negatively influence fighting behavior in animals.