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.      

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.     

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.     

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.       

Neighbour-stranger song discrimination in territorial ortolan bunting Emberiza hortulana males

Neighbour-stranger discrimination has been demonstrated in many species, but the mechanisms employed in discrimination vary. We tested whether an oscine bird with small repertoire size, the ortolan bunting Emberiza hortulana , discriminated between songs of neighbours and strangers. We performed playback experiments to measure response of males to a repeated single example of a single song type derived from a repertoire of a neighbour or stranger. Thirteen males were tested twice each, and in both cases songs were broadcast from the territory boundary shared by the subject male and the neighbour. Subjects responded more aggressively to songs of strangers than neighbours, i.e. they approached the loudspeaker faster and came closer and did more flights during the playback of stranger song. We found no significant differences in vocal response between treatments. We conclude that ortolan bunting can discriminate between songs of neighbours and strangers. This study provides experimental evidence for ortolan buntings in neighbour-stranger discrimination. It also demonstrates that a single example of song is enough to discriminate between neighbours and strangers. We discuss which song characteristics are the possible acoustic basis for discrimination in the studied species.     

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.     

Sex Discrimination via Anal Gland Secretion in a Territorial Monogamous Mammal

Monogamy in mammals is relatively unusual, only occurring in 3–5% and to an even lesser degree in rodents. Monogamy exists in two forms, facultative which evolved due to female dispersion and obligate when male care is needed for offspring survival. Most monogamous rodents use scent marking as a form of territorial defence to obtain exclusive access to vital resources. Intrasexual competition occurs in many species to maintain pair bonds and also to signal presence within a territory. In this study, we tested the hypothesis that resident obligate monogamous Eurasian beaver (Castor fiber) can discriminate between the sexes when investigating anal gland secretions (AGS) from unknown (stranger) mated pairs. We predicted that, due to intrasexual competition, dominant territorial male and female beavers will display a stronger response to AGS of same‐sex conspecifics. Territorial intrusion by mated pair strangers was simulated by the formation of experimental scent mounds (ESM) with AGS. Our results showed that both sexes (1) displayed a stronger response to the male AGS in sniffing duration, (2) physically responded for longer durations towards male AGS and (3) overmarked male AGS more frequently. We infer that obligate monogamous mammals can determine the sexual identity of intruding conspecifics of a mated pair via AGS and that intruding males may pose more of a threat to resident males via intrasexual competition and resident females due to the long‐term costs, such as infanticide and abortion, of a new dominant male.     

'Nasty neighbours' rather than 'dear enemies' in a social carnivore

Territorial animals typically respond less aggressively to neighbours than to strangers. This 'dear enemy effect' has been explained by differing familiarity or by different threat levels posed by neighbours and strangers. In most species, both the familiarity and the threat-level hypotheses predict a stronger response to strangers than to neighbours. In contrast, the threat-level hypothesis predicts a stronger response to neighbours than to strangers in species with intense competition between neighbours and with residents outnumbering strangers, as commonly found in social mammals such as the banded mongoose (Mungos mungo). The familiarity hypothesis predicts reduced aggression towards neighbours also in these species. We exposed free-living banded mongoose groups to translocated scent marks of neighbouring groups and strangers. Groups vocalized more and inspected more samples in response to olfactory cues of the neighbours than to the strangers. Our results support the threat-level hypothesis and contradict the familiarity hypothesis. We suggest that increased aggression towards neighbours is more common in social species with intense competition between neighbours, as opposed to reduced aggression towards neighbours typical for most solitary species.     

Individual voice recognition in a territorial frog (Rana catesbeiana)

Some territorial animals display low levels of aggression towards a familiar territorial neighbour in its usual territory, but exhibit high levels of aggression towards neighbours in novel locations and unfamiliar individuals. Here, we report results from a field playback study that investigated whether territorial males of the North American bullfrog (Rana catesbeiana) could discriminate between the acoustic signals of simulated neighbours and strangers in the absence of contextual cues associated with a specific location. Following repeated exposures to synthetic bullfrog calls from a particular location, subjects responded significantly less aggressively to a familiar call, compared with an unfamiliar one, when both calls were broadcast from familiar and novel locations, indicating that bullfrogs could recognize a neighbour's calls independently of the contextual cues provided by the direction of the neighbour's territory. Subjects responded equally aggressively to unfamiliar calls broadcast from either a familiar or a novel location, which indicates that they could perceive unfamiliar calls as those of a stranger, regardless of where the stranger was encountered. Together, these two results provide evidence that a frog possesses a capacity for individual voice recognition.     

Interspecific variation in neighbour–stranger discrimination in ants of the Neoponera apicalis complex

1. The ecological success of social insects lies in their ability to prevent the exploitation of colony resources by competitors or parasites. Nestmate recognition is therefore of crucial importance in maintaining the integrity of the colony. Furthermore, inter‐colony competitive relationships are often complex, as many species discriminate between neighbours and strangers, with reduced (the dear enemy phenomenon) or increased levels of aggression towards nearby colonies, depending on the species. In this context, between‐species comparisons could be particularly helpful to investigate the proximate causes underlying this context‐dependent phenomenon, but these are notoriously lacking. 2. Here an attempt was made to circumvent this drawback by studying three closely related sympatric ant species with very similar life histories that belong to the Neoponera apicalis complex. The present study investigated how nestmate recognition and inter‐colony competitive relationships were influenced by spatial, chemical and genetic distances between colonies. 3. It was found that one species, N. apicalis morph 7, showed a clear dear enemy phenomenon with no influence of chemical and genetic distances, suggesting the existence of a learning process. In contrast, N. apicalis morph 4 and Neoponera verenae morph 1 failed to show any strong discrimination between close and distant non‐nestmates. 4. These results are discussed in the light of the observed interspecific variation in nesting preferences, possibly constraining the opportunities of familiarisation between nearby nests, and modulating the competition for resources between colonies. 5. It is argued that this study further reinforces the relative threat level hypothesis as an ultimate explanation for neighbour–stranger discrimination processes.     

MICRODIALECT AND GROUP SIGNATURE IN THE SONG OF THE SKYLARK ALAUDA ARVENSIS

ABSTRACT

The Skylark Alauda arvensis is a territorial species of open landscape in which pairs settle in stable and adjacent territories during the breeding season. Due to the heterogeneity of the habitat, territories are gathered in patches spaced by a few kilometres, in which each male produces very long and complex flight songs as a part of the territorial behaviour. We showed that, in a given patch, all the males (neighbours) share some particular sequences of syllables in their songs, whereas males settled in different patches (strangers) have almost no sequences in common. Such a phenomenon is known as microdialect. To test the hypothesis that these shared sequences support a group signature, we made playback experiments with “chimeric” signals: songs of strangers where the sequences shared by neighbours were artificially inserted. Behavioural responses to playbacks indicated a neighbour-stranger discrimination consistent with the dear enemy phenomenon, i.e. a reduced aggression toward neighbours compared to strangers. Furthermore, the same level of responses, observed when a “chimeric” song and a neighbour song were broadcast, indicated that shared sequences are recognised and identified as markers of the neighbourhood identity.     

Neighbor–Stranger Discrimination in Concave-Eared Torrent Frogs, Odorrana tormota

The dear enemy phenomenon in which animals discriminate familiar neighbors from unknown strangers, and respond more aggressively to strangers is well established in various social animals, especially in songbirds and mammals. So far, very few studies of neighbor–stranger discrimination have been carried out in amphibians and the results have been mixed. Thus, it is unclear whether this phenomenon exists commonly in frogs and toads, and whether it is exhibited by species with large vocal repertoires. We conducted acoustic playback experiments with male concave-eared torrent frogs ( Odorrana tormota , a species with an unusually large vocal repertoire) kept in a tank in a quiet room to investigate whether or not they can discriminate strangers from neighbors acoustically. Nine of the 14 males tested showed evoked vocal responses to the calls from strangers, but none to calls from neighbors; vocal response to the calls from strangers was accompanied by aggressive motor activity. These results demonstrate that male O. tormota possess the ability to discriminate neighbors from strangers acoustically. Odorrana tormota therefore joins three ranid species ( Rana catesbiana , Rana clamitans , Rana dalmatina , all known to have a comparatively small and stereotyped vocal repertoires) as the only anurans demonstrated to have this ability. Given the difference in signaling complexity between these frog species, the salient acoustic features used for discriminating neighbors and strangers are likely to be quite distinct.     

Duet codes do not enhance neighbour recognition in two closely related species of duetting neotropical wrens

Numerous studies have shown that territorial animals exhibit less aggression in response to neighbours than to strangers, a phenomenon known as dear enemy effect. The influence of acoustic features, such as song type sharing and repertoire sizes, in neighbour recognition has been widely documented in male songbirds. However, few studies have focused on duetting species, and particularly on those where pairs have pair‐specific duet codes (consistent associations of their individual phrase types). Given that each pair in the population can have a unique repertoire of duet types, duet codes have been hypothesized to enhance discrimination. In this context, we tested for evidence of neighbour recognition and duet code discrimination in two closely related species of neotropical wrens, the riverside wren, Cantorchilus semibadius, and the canebrake wren, C. modestus zeledoni. Although both species have moderately large repertoires, riverside wrens have higher levels of phrase type and duet type sharing across the population. We compared the approach and vocal responses of focal pairs to three playback treatments: neighbours' correct duet type, neighbours' incorrect duet type and a strangers' duet type. We found that riverside wrens displayed a stronger response to the strangers' playback than to both neighbours' playbacks, whereas no differences among treatments were found in canebrake wrens. Given that both species exhibited similar levels of aggression during neighbour playbacks, regardless of whether the correct duet code was used, our findings suggest duet codes do not facilitate neighbour recognition. We conclude that the function of duet codes in these species might be more closely related to intra‐pair communication. Finally, we suggest that the level of dear enemy effect a species exhibits depends on ecological factors that influence the perceived level of threat of territory intruders.     

Juvenile Richardson's Ground Squirrels (Spermophilus richardsonii) Manifest Both Littermate and Neighbour/Stranger Discrimination

Newborn ground squirrels (Spermophilus spp.) are reared in isolation of individuals belonging to other litters. At or near weaning, they broaden their social interactions to encompass conspecifics other than littermates. In laboratory studies, juvenile ground squirrels commonly discriminate littermates from non-littermates, but few studies have examined whether behavioural discrimination at that level persists under natural circumstances. Previous studies have also all but ignored the possibility of alternative levels of social discrimination augmenting or replacing the discrimination of littermates from non-littermates. To examine those possibilities, I staged interactions in a neutral arena between littermate, neighbour and non-neighbour (stranger) pairs of otherwise free-living juvenile Richardson's ground squirrels (Spermophilus richardsonii). Littermates interacted more frequently than other pair types and showed the highest proportion of cohesive behaviour and the least agonism. Strangers interacted less frequently than all other pair types, showed the fewest recognitive contacts, and were the least cohesive and most agonistic. Neighbours interacted less than littermates, but more than strangers, and showed intermediate levels of cohesion and agonism. Neighbours also engaged in more recognitive contacts than strangers, but did not have fewer recognitive contacts than littermates. Defecation rates also differed among interactant types: littermates left the fewest scats in the arena, neighbours deposited an intermediate number and strangers defecated the most. My results substantiate those of earlier laboratory studies suggesting that the discrimination of littermates from neighbouring juveniles persists in the natural context. These data also extend those earlier findings by demonstrating that juveniles come to discriminate neighbours from strangers. Comparisons of the behaviour of related vs. unrelated neighbours reveal that neighbour/stranger discrimination is contingent upon differential familiarity. Simultaneous social discrimination at the levels documented could promote kin-biased behaviour and cooperation among both related and unrelated neighbours.     

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.     

Scent‐marking behavior by subordinate Eurasian beavers

Chemical communication by scent‐marking is widespread among mammals and can serve different purposes, such as territory demarcation, mate attraction and self‐advertisement. In this study, we examined scent‐marking behavior by subordinate Eurasian beavers (Castor fiber) in a population in southeast Norway. We conducted scent experiments in 18 family groups, simulating a territory intruder using experimental scent mounds (ESM). In total, we recorded 196 territorial reactions (destroying and/or overmarking of scent mounds). Subordinates contributed 14% of all territorial reactions and first overmarked 12% of the ESM, and the number of subordinates in the family group did not increase the total number of territorial reactions. This suggests that the contribution by subordinates plays a minor role in territorial defense. The number of territorial reactions by subordinates was positively related to the age of their parents, suggesting that subordinates might take over territorial duties with increasing parental senescence, likely because they have increased chances of inheriting the territory. Increased experience in territorial activities possibly helps subordinates to successfully gain and defend a territory of their own.     

Are Unfamiliar Neighbours Considered to Be Dear-Enemies?

Background

Discriminating threatening individuals from non-threatening ones allow territory owners to modulate their territorial responses according to the threat posed by each intruder. This ability reduces costs associated with territorial defence. Reduced aggression towards familiar adjacent neighbours, termed the dear-enemy effect, has been shown in numerous species. An important question that has never been investigated is whether territory owners perceive distant neighbours established in the same group as strangers because of their unfamiliarity, or as dear-enemies because of their group membership.

Methodology/Principal Findings

To investigate this question, we played back to male skylarks (Alauda arvensis) songs of adjacent neighbours, distant neighbours established a few territories away in the same microdialect area and strangers. Additionally, we carried out a propagation experiment to investigate how far skylark songs are propagated in their natural habitat and we estimated repertoire similarity between adjacent neighbours, distant neighbours and strangers. We show that skylarks, in the field, respond less aggressively to songs of their distant and likely unfamiliar neighbours, as shown by the propagation experiment, compared to stranger songs. The song analysis revealed that individuals share a high amount of syllables and sequences with both their adjacent and distant neighbours, but only few syllables and no sequences with strangers.

Conclusions

The observed reduction of aggression between distant neighbours thus probably results from their familiarity with the vocal group signature shared by all members of the neighbourhood. Therefore, in skylarks, dear-enemy-like relationships can be established between unfamiliar individuals who share a common acoustic code.     

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.     

Potential risks of olfactory signaling: the effect of predators on scent marking by beavers

Mammals scent mark their territories to advertise occupancyand ownership. However, signaling with scent for territorialdefense can have a negative effect by advertising an individual'spresence and location to predators. In this study, we measuredresponses to a simulated territorial intrusion by conspecificadult male Eurasian beavers (Castor fiber) either in the localizedpresence or in the absence of odor of a predator to test thehypothesis that the territorial defense of free-living beaverswould be disrupted by the presence of predation risk in theirnatural environment. We predicted that beavers would significantlyreduce their willingness to countermark intruder's scent inthe presence of the scent of predators (wolf [Canis lupus] andlynx [Lynx lynx]), compared with a control (no odor), as responsesare in general stronger to predator scent marks than nonpredatorscent. Therefore, we also predicted that the effects of nonpredatorymammal scent (neophobic control) (eland [Taurotragus oryx] andhorse [Equus cabalus]) are to be expected somewhere in betweenthe effects of the predator odor and a control. Our resultssuggest that both predator and nonpredator scents reduce beaversresponse to a simulated intruder's scent mounds and thereforedisrupt their territorial defense. However, predator scent hada stronger effect than nonpredator scent. Beavers may thereforebe at great risk on territories with predators present becauseof the trade-off between predator avoidance and territorialdefense. Our study demonstrates the potential of predation riskas a powerful agent of counterselection on olfactory signalingbehavior.     

Otter scent signals age, sex, and reproductive status

Scent is used across taxa to communicate information about signaler identity. Eurasian otters Lutra lutra are mainly solitary and thought to use scent as their primary means of communication. Little is known, however, about what information otters communicate through scent or what social function this performs. Headspace solid-phase microextraction and gas chromatography-mass spectrometry were used to sample and analyze volatile organic compounds from anal scent gland secretion from 158 otters of differing sex, age, and female reproductive status. Univariate and multivariate differences were clear between adult and juvenile otters. Complex sex differences were apparent in adult otters but not in younger individuals, suggesting the use of this scent secretion in mate attraction. The scent of pregnant and lactating females was highly differentiated from male and juvenile scent, but anecdotal reports suggest females avoid communication during these times.