Dear Enemies Elicit Lower Androgen Responses to Territorial Challenges than Unfamiliar Intruders in a Cichlid Fish

In many territorial species androgen hormones are known to increase in response to territorial intrusions as a way to adjust the expression of androgen-dependent behaviour to social challenges. The dear enemy effect has also been described in territorial species and posits that resident individuals show a more aggressive response to intrusions by strangers than by other territorial neighbours. Therefore, we hypothesized that the dear enemy effect may also modulate the androgen response to a territorial intrusion. Here we tested this hypothesis in male cichlid fish (Mozambique tilapia, Oreochromis mossambicus) using a paradigm of four repeated territorial intrusions, either by the same neighbour or by four different unfamiliar intruders. Neighbour intruders elicited lower aggression and a weaker androgen response than strangers on the first intrusion of the experiment. With repeated intrusions, the agonistic behaviour of the resident males against familiar intruders was similar to that displayed towards strangers. By the fourth intrusion the androgen response was significantly reduced and there was no longer a difference between the responses to the two types of intruders. These results suggest that the dear enemy effect modulates the androgen response to territorial intrusions and that repeated intrusions lead to a habituation of the androgen response.     

Behavioral response to familiar and unfamiliar neighbors in a territorial cichlid, <Emphasis Type="Italic">Neolamprologus pulcher</Emphasis>

Some territorial species have been shown to react more aggressively toward unfamiliar conspecifics than established neighbors, a behavior referred to as the dear enemy phenomenon. Laboratory experiments were conducted to determine whether males of a territorial African cichlid, Neolamprologus pulcher, can discriminate between size-matched familiar and unfamiliar male neighbors and whether they respond more aggressively toward unfamiliar males. It was found that males spent significantly more time near the territorial boundary that they shared with unfamiliar neighbors and directed significantly more aggressive behavior toward these individuals.     

When are neighbours ‘dear enemies’ and when are they not? The responses of territorial male variegated pupfish, Cyprinodon variegatus, to neighbours, strangers and heterospecifics

Dear enemy recognition reduces the costs of territorial defence in some species, but not others, when a neighbour is more threatening to a resident's fitness than an intruder. I asked whether dear enemy effects were fixed in a particular species, or if the reduced aggression between a resident and neighbour was disrupted by the presence of potential mating opportunities. Observing variegated pupfish, Cyprinodon variegatus, in the field and in the laboratory, I examined the effects of a female's presence in a male's territory on residents' aggressive responses to conspecific neighbours and strangers as well as heterospecific opponents. Although reduced aggression consistent with dear enemy recognition was seen between conspecific neighbours in the absence of females, the presence of a female in a male's territory instigated comparably greater aggression between the neighbours. No reduction in aggression was seen between pupfish males and heterospecific opponents. These findings suggest that dear enemy recognition may be a flexible, rather than a fixed, feature of the relationship of neighbouring conspecific males. Despite the disruption in dear enemy recognition caused by a female, residents in the laboratory faced with neighbours spent more time associating with the female than residents faced with strangers. This allowed the residents to secure as many spawns as did males who had been faced with no competitor. Residents faced with any other type of opponent had reduced reproductive success, suggesting that the dear enemy relationship between residents and neighbours is more complex than simply a reduction in aggression. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.       

Seasonal Variation in Response to Neighbors and Strangers by a Territorial Songbird

Reduced aggression toward territorial neighbors, termed the ‘dear‐enemy’ effect, is thought to arise because territorial animals benefit by avoiding contests with neighbors with whom they have already established relationships. The dear‐enemy effect has been described in many taxa, but few studies have considered whether or not neighbors’ relationships are affected by changes in the social environment. In this study, I tested whether Carolina wrens, Thryothorus ludovicianus, behaviorally discriminate between neighbors and strangers in two different social environments: in spring when territories have been established for several months, and in fall when an influx of new birds claiming territories might de‐stabilize wren neighborhoods. Comparisons of responses of territorial males to playbacks of songs from neighbors and strangers showed that Carolina wrens show the dear‐enemy effect in spring, but not in fall in this design. The apparent lack of a differential response to neighbors and strangers in fall might be due to a reduction in aggression toward strangers. This study provides evidence that seasonal changes in the dear‐enemy effect coincide with seasonal changes in the social environment.     

The Influence of Relatedness, Neighbourhood and Overall Distance on Colony Mate Recognition in a Polydomous Ant

The ‘dear enemy phenomenon’ predicts that territorial animals respond less aggressively towards more familiar neighbours than towards unfamiliar conspecifics if potential losses to strangers are more costly than potential losses to neighbours. Conversely, territorial animals should respond more aggressively to neighbours, if potential losses to them are more costly than potential losses to strangers. In social insects the question of how colony members distinguish neighbours from strangers, however, is intertwined with the more general question of how colony members discriminate themselves from non‐colony members; both genetic and spatial distance can correlate with levels of inter‐colonial aggression. In this paper I disentangle the role of experience, genetic and spatial distance on inter‐colonial aggression in a polydomous population of Iridomyrmex purpureus. In I. purpureus, aggression is related to the spatial distance between colonies irrespective of genetic similarity. Spatial distance affected aggression in two different ways. First, workers were more likely to exhibit aggression towards alien conspecifics of adjoining rather than non‐adjoining territories, suggesting the opposite of the dear enemy phenomenon. Second, workers were more often aggressive towards conspecifics of more distant colonies, implying that environmental cues play a role in the recognition system of I. purpureus.     

Effects of previous experience on the agonistic behaviour of male crickets, Gryllus bimaculatus

Male solitary animals frequently enter aggressive interactions with conspecific individuals to protect their territory or to gain access to females. After an agonistic encounter, the loser (subordinate individual) changes its behaviour from aggression to avoidance. We investigated agonistic interactions between pairs of male crickets to understand how dominance is established and maintained. Two na?ve males readily entered into agonistic interactions. Fights escalated in a stereotyped manner and were concluded with the establishment of dominance. If individuals were isolated after the first encounter and placed together 15 minutes later, subordinate crickets tended to avoid any further contact with the former dominant opponent. Moreover, subordinate males also avoided unfamiliar dominant and na?ve opponents. They displayed aggressive behaviour only towards unfamiliar subordinate opponents. This suggests that the subordinate male change their behaviour depending on the dominance status of the opponent. Dominant crickets, in contrast, displayed aggressive behaviour towards familiar as well as unfamiliar opponents. If the interval between the first and second encounter was longer than 30 minutes, the former subordinate male showed aggressive behaviour again. However, if the subordinate cricket was paired with the same opponent three consecutive times within 45 minutes, it avoided the former dominant opponent for up to 6 hours following the third encounter. Our results suggest that the maintenance of dominance in male crickets depends largely on the behavioural change of subordinate individuals. Possible mechanisms to maintain dominance are discussed.     

Male <Emphasis Type="Italic">Betta splendends</Emphasis> are equally aggressive toward neighbors and strangers

Male Siamese fighting fish, Betta splendens, are known for their ferociousness when defending their territories against male or female conspecific intruders. The aim of this study was to investigate whether this species exhibits the dear enemy phenomenon, where territorial males would be less aggressive toward neighbors with already established territories than toward complete stranger males. In experiment 1, a male Betta was placed in an aquarium. A second male was placed in a glass jar that was fitted in one corner of the aquarium. After 24 h, a cover was placed around the jar, and then removed after 1 h. Alternatively, the jar male was replaced with a different male of a different color while the jar was covered. The frequency and duration of opercular expansion by the aquarium male were recorded. In experiment 2, two male Bettas were placed, each in a half of a large aquarium that was equally divided by a clear, perforated Plexiglas divider. After 24 h, one male (intruder) was transferred into the other male’s (resident) half. In another variation of the experiment, the intruder was a stranger male Betta that the resident male had never encountered before. The opercular expansion and duration were scored for the resident male. The results indicated that male Siamese fish reacted similarly to familiar and stranger males. This lack of dear enemy effect in Siamese fish could be due to an inability to discriminate between neighboring males and non-neighboring males. Alternatively, territorial males could be equally aggressive to all intruders because all intruders represent equal danger.     

Effects of territorial intrusions on eavesdropping neighbors: communication networks in nightingales

Animal communication often occurs in communication networksin which multiple signalers and receivers are within signalingrange of each other. In such networks, individuals can obtaininformation on the quality and motivation of territorial neighborsby eavesdropping on their signaling interactions. In songbirds,extracting information from interactions involving neighborsis thought to be an important factor in the evolution of strategiesof territory defense. In a playback experiment with radio-taggednightingales Luscinia megarhynchos we here demonstrate thatterritorial males use their familiar neighbors' performancein a vocal interaction with an unfamiliar intruder as a standardfor their own response. Males were attracted by a vocal interactionbetween their neighbor and a simulated stranger and intrudedinto the neighbor's territory. The more intensely the neighborhad interacted with playback, the earlier the intrusions weremade, indicating that males eavesdropped on the vocal contestinvolving a neighbor. However, males never intruded when wehad simulated by a second playback that the intruder had retreatedand sang outside the neighbor's territory. These results suggestthat territorial males use their neighbors' singing behavioras an early warning system when territorial integrity is threatened.Simultaneous responses by neighboring males towards unfamiliarrivals are likely to be beneficial to the individuals in maintainingterritorial integrity.     

Adult male collared lizards, Crotaphytus collaris, increase aggression towards displaced neighbours

Differential responses to neighbours and strangers (the dear enemy phenomenon) and individual recognition presumably evolve to reduce costs of territorial defence. Territorial residents have been found to demonstrate reduced aggression towards neighbours wherever they are encountered along that resident's territory boundary except for when the neighbour is displaced to the boundary opposite the shared boundary. In this new location, the displaced neighbour represents a greater threat to the resident's territory ownership, and should be treated as equally aggressive as a stranger. Finding increased aggression towards displaced neighbours has been interpreted as individual recognition, but these results do not provide sufficient evidence to rule out the possibility that the resident sees the neighbour out of its normal context as just another stranger. We tested the hypothesis that territorial collard lizards can individually recognize neighbours and will increase aggression towards them as the threat to territorial ownership increases. Resident males treated neighbours that had been moved to the opposite boundary as equally aggressive as strangers. However, residents responded more aggressively towards strangers than towards neighbours on natural territories (the dear enemy phenomenon) and also in neutral arena encounters. Our results suggest that resident male collared lizards are able to recognize individuals regardless of context and respond to them according to the threat that they pose. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Relative threat and recognition ability in the responses of tropical mockingbirds to song playback

It has been suggested that individual recognition based on song may be constrained by repertoire size in songbirds with very large song repertoires. This hypothesis has been difficult to test because there are few studies on species with very large repertoires and because traditional experiments based on the dear enemy effect do not provide evidence against recognition. The tropical mockingbird, Mimus gilvus, is a cooperative breeder with very large song repertoires and stable territorial neighbourhoods. The social system of this species allowed us to test individual recognition based on song independently from the dear enemy effect by evaluating male response to playback of strangers, neighbours (from shared and unshared boundaries), co-males (i.e. other males in the same social group) and own songs. Although subjects did not show a dear enemy effect, they were less aggressive to co-males than to all other singers. Our results suggest that recognition in tropical mockingbirds (1) does not simply distinguish between familiar and unfamiliar singers, (2) requires a small sample of both songs and song types, (3) does not rely on individual-specific sequences of song types and (4) is not likely to rely on group-specific vocal signatures potentially available in cooperatively breeding groups. We conclude that this is a case of true recognition and suggest that the lack of a dear enemy effect in this and other species with large repertoires may relate to the role of song in mate attraction and the perception of neighbours as a threat to future paternity.     

Male song sparrows have elevated testosterone in response to neighbors versus strangers

Upon hearing a conspecific signal, animals must assess their relationship with the signaller and respond appropriately. Territorial animals usually respond more aggressively to strangers than neighbors in a phenomenon known as the “dear enemy effect”. This phenomenon likely evolved because strangers represent a threat to an animal's territory tenure and parentage, whereas neighbors only represent a threat to an animal's parentage because they already possess a territory (providing territory boundaries are established and stable). Although the dear enemy effect has been widely documented using behavioral response variables, little research has been conducted on the physiological responses of animals to neighbors versus strangers. We sought to investigate whether the dear enemy effect is observed physiologically by exposing territorial male song sparrows (Melospiza melodia) to playback simulating a neighbor or a stranger, and then collecting blood samples to measure plasma testosterone levels. We predicted that song sparrows would exhibit increased testosterone levels after exposure to stranger playback compared to neighbor playback, due to the role testosterone plays in regulating aggression. Contrary to our prediction, we found that song sparrows had higher testosterone levels after exposure to neighbor playback compared to stranger playback. We discuss several explanations for our result, notably that corticosterone may regulate the dear enemy effect in male song sparrows and this may inhibit plasma testosterone. Future studies will benefit from examining corticosterone in addition to testosterone, to better understand the hormonal underpinnings of the dear enemy effect.     

The effect of familiarity on social interactions in meadow voles,Microtus pennsylvanicus: a laboratory and field study

The role of familiarity in affecting the outcome of social interactions among meadow voles was investigated in both a laboratory and a field experiment. In the laboratory, captive meadow voles, Microtus pennsylvanicus, were exposed to a conspecific's odour. The voles were then placed into two groups: familiar and unfamiliar. Familiar voles were individuals who underwent staged dyadic encounters with the conspecific to whose odours they had been exposed. Unfamiliar voles were individuals who underwent paired encounters with conspecifics to whose odours they had not been exposed. In the field experiment, familiar voles were neighbours that were trapped within each other's home ranges over two consecutive bi-weekly trapping sessions. Unfamiliar voles were individuals that were trapped on different trapping grids. The results of the laboratory and field studies were similar. Encounters between familiar females resulted in less agonistic behaviour and more amicable acts than encounters between unfamiliar females. In contrast, encounters between familiar males resulted in more agonistic behaviour than encounters between unfamiliar males. Familiarity did not affect the outcome of male-female interactions. These results are discussed in the framework of the social system of the meadow vole.     

Rival recognition in the territorial tawny dragon (Ctenophorus decresii)

The ability to discriminate between familiar and unfamiliar conspecifics is important in territorial animals as it allows animals to distinguish neighbours from non-neighbours. This prevents wasting time and energy in unnecessary aggressive interactions. I investigated the ability of adult males of a territorial lizard, the tawny dragon (Ctenophorus decresii), to distinguish familiar from unfamiliar rivals in a laboratory setting. Males significantly reduced their aggression levels in repeat interactions with familiar rivals and increased their aggression levels towards unfamiliar males. The time taken for interactions to be settled was also significantly lower towards familiar than unfamiliar males. The results of this study suggest that adult male tawny dragons can discriminate familiar from unfamiliar conspecifics. Furthermore, animals were presented with three new rivals in succession and showed a robust ability to discriminate between familiar and unfamiliar males.     

Parasitized Salamanders are Inferior Competitors for Territories and Food Resources

Parasites have been shown to impair the behaviour of their hosts, compromising the host's ability to exploit and compete for resources. We conducted two experiments to determine whether infestation with an ectoparasitic mite (Hannemania eltoni) was associated with changes in aggressive and foraging behaviour in the Ozark zigzag salamander, Plethodon angusticlavius. In a first experiment, male salamanders with high parasite loads were less aggressive overall than males with low parasite loads during territorial disputes. In addition, males with high parasite loads were more aggressive toward opponents with high parasite loads (symmetric contests) than toward opponents with low parasite loads (asymmetric contests). In contrast, males with low parasite loads did not adjust their level of aggression according to the parasite load of the opponent. In a second experiment, foraging behaviour of females was tested in response to ‘familiar’ (Drosophila) prey and ‘novel’ (termite) prey. Latency to first capture was significantly longer for parasitized than non‐parasitized females when tested with ‘familiar’ prey, but not for ‘novel’ prey. Our results suggest that parasite‐mediated effects may have profound influences on individual fitness in nature.     

Sexual dimorphism in responses to unfamiliar intruders in the tamarin, Saguinus oedipus

Aspects of social structure in group-living species can be inferred by observing the responses of individuals to unfamiliar animals. This study examined the responses of mated pairs of cotton-top tamarins (Saguinus oedipus oedipus) to presentation of either unfamiliar conspecifics or members of a related tamarin species, the saddle-back tamarin (Saguinus fuscicollis fuscicollis). Male and female responses to intruders differed: resident males threatened, displayed piloerection, approached, and attacked intruders, especially males, while resident females showed increases in suprapubic scentmarking in the presence of intruders. Both males and females discriminated between the species of intruders, exhibiting more threats, scent-marking, piloerection, and approaches in the presence of conspecific intruders. There are pronounced sex differences in the signals and behaviour patterns that are elicited in an aggressive or territorial encounter with unfamiliar conspecifics in this monogamous primate.     

Social status influences microhabitat selection: breeder and floater Eagle Owls Bubo bubo use different post sites

Social status can be reflected in many aspects of an individual’s behaviour and ecology, including habitat use and conspecific interactions. In territorial species where at least two social groups – breeding birds and non‐territorial floaters – are recognized, the diverse tasks associated with territorial ownership can lead territory holders to behave differently from the non‐territorial part of the population. Territory holders defend their breeding area and reproduce, whereas floating individuals are dispersing and lead a more transient life, during which they do not show any territorial behaviour even when settling in a more or less fixed area (known as the stop phase). As social interactions are based on visual and vocal cues, the use of specific sites for sending and/or receiving signals can be a crucial choice in an animal’s life. By analysing the post‐site selection of Eagle Owl Bubo bubo breeders and floaters during their nocturnal activity, we found that: (1) territory holders selected more visible and dominant posts than non‐territorial floaters; (2) the choice of posts made by floating individuals did not differ between the wandering and stop phases of dispersal; and (3) floating females intruded more frequently than floating males within a breeder’s home‐range. These findings highlight the fact that two social strategies are possible within the same species, depending on an individual’s social status and its related tasks. Breeders could take advantage of visible locations to declare their status as territory holders, whereas floaters could benefit from a more secretive life to wander unnoticed among occupied territories. This secretive life would help floaters to reduce the risks associated with conspecific aggression. Finally, the greater occurrence of floating females within breeders’ home‐ranges can be explained by the fact that female incursions in a breeder’s home‐range are less risky than male intrusions.     

Agonistic display or courtship behavior? A review of contests over mating opportunity in butterflies

Male butterflies compete over mating opportunities. Two types of contest behavior are reported. Males of various butterfly species compete over a mating territory via aerial interactions until one of the two contestants retreats. Males of other butterfly species fly around larval food plants to find receptive females. Males of some species among the latter type can find a conspecific pupa, and they gather around it without expelling their rivals. Scramble competition over mating occurs when a female emerges from the pupa. Many studies have been performed on territorial species, and their contest resolution has often been understood from the point of view of contest models based on game theory. However, these models cannot explain why these butterflies perform contest displays despite the fact that they do not have the ability to attack their opponent. A recent study based on Lloyd Morgan’s Canon showed that territorial contests of male butterflies are better understood as erroneous courtship between sexually active males. In this paper, I review research on contests over mating opportunity in butterflies, and show that the erroneous courtship framework can explain not only territorial contests of butterflies but also why males do not determine the owner of a conspecific pupa.     

Disruption of Dear Enemy Recognition Among Neighboring Males by Female Leon Springs pupfish, Cyprinodon bovinus

Males defending territories often settle into adjacent areas, sharing a common border that is maintained by a reduced level of aggression known as dear enemy recognition. While social conditions may affect the dear enemy relationship among males, what role females play, if any, is unclear. In a field study of the highly promiscuous Leon Springs pupfish, Cyprinodon bovinus, we asked whether females influenced this relationship of neighbors to their advantage. We observed 16 territorial residents, mapping the precise location of each male's behaviors within its territory. Resident males engaged in less aggression against neighbors compared with intruders, and neighbors intruded less deeply into the residents’ territories than intruders. Despite this locality restriction, neighbors were responsible for as many spawning interruptions as intruders. Females did not spawn randomly in the males’ territories, nor did they spawn near territory centers where aggression was low. Rather, females were more likely to settle and spawn in the outer half of the territories where competition among males was highest. When a neighbor entered a resident's territory to interrupt a spawn, the female was more likely to leave the resident's territory for the neighbor's than to remain. These observations suggest that the female used the intrusion by the neighbor to engage the resident and interrupt the spawn as a measure of this male's quality and that, while neighboring males benefit from the presence of dear enemy recognition, females benefit from its disruption.     

Anti-predator behaviour changes following an aggressive encounter in the lizard Tropidurus hispidus

Avoiding predators may conflict with territorial defence because a hiding territorial resident is unable to monitor its territory or defend it from conspecific intrusions. With persistent intruders, the presence of an intruder in the near past can indicate an increased probability of future intrusions. Therefore, following a conspecific-intrusion, territorial residents should minimize costs from future intrusions at the cost of higher predation risks. I conducted experiments with males of the territorial lizard Tropidurus hispidus recording approach distance (distance between predator and prey when the prey escapes) and time to re-emergence from a refuge after hiding. Past aggressive interactions affected anti-predator behaviour: lizards re-emerged sooner (compared to a control) when the predator attacked 5 min after an aggressive encounter. If the predator attacked while an aggressive encounter was ongoing, there was also a reduction in approach distance. The results are consistent with an economic hypothesis which predicts that T. hispidus incur greater predation risks to minimize future territorial intrusion; additionally they show that the effects of past and ongoing aggressive interactions are different, consistent with the minimization of present intrusion costs. These results are relevant for studies of the changes in aggressive behaviour due to changes in the social environment and for studies of the costs and (co) evolution of aggressive and anti-predator strategies.     

Do competing males cooperate? Familiarity and its effect on cooperation during predator inspection in male three‐spined sticklebacks (Gasterosteus aculeatus)

We investigated the trade‐off between conflict and cooperation, using predator inspection behaviour in sticklebacks as a model system. Male three‐spined sticklebacks ( Gasterosteus aculeatus ) compete for territories during the breeding season and it has been demonstrated that the level of aggression between territorial neighbours declines with time, a phenomenon known as the dear enemy effect. In this experiment we examine whether this increase in familiarity between territorial neighbours can facilitate an increase in cooperation during predator inspection events. This was analyzed using male sticklebacks from four pond populations, two with and two without predatory rainbow trout ( Oncorhyncus mykiss ). Males were each exposed to five different treatments: (1) the presentation of a live rainbow trout when alone; (2) with a newly revealed territorial neighbour; (3) with this neighbour after two days of familiarization; (4) with another unfamiliar neighbour (termed a 'floater'); and (5) a second solitary trial (to provide controls at the start and end of the experiment). As predicted, fish from predator‐sympatric populations showed higher levels of predator inspection and lower rates of misdirected territorial aggression towards the predator throughout. However, familiarity between neighbouring males did not facilitate an increase in predator inspection behaviour. Instead, predator inspection behaviour decreased throughout treatments involving the presence of any sort of neighbouring male. Familiarity between neighbours did not influence their ability to cooperatively inspect, but only the nature of any aggressive territorial behaviours, all of which detracted equally from individual inspection effort.