Territorial intrusion risk and antipredator behaviour: a mathematical model

In territorial animals that hide to avoid predators, a predatory attack creates a conflict because a hiding animal cannot defend its territory from conspecific intruders. When intruders are persistent, a past conspecific intrusion informs a territorial resident that future intrusions by the same animal are likely. Using a mathematical model, I examine the effects that past territorial intrusions can have on antipredator behaviour. Past territorial intrusions rarely affect a resident animal's time to hide (the optimal behaviour is to hide as soon as the predator initiates its attack). In contrast, past intrusions should shorten the length of time during which territory holders remain in hiding, with the magnitude of this effect depending on the time of the predator's attack, the re-intruder's pattern of return, and the intrusion rates of other conspecifics. The results of the model show that we need more information on patterns of re-intruders' behaviour, and emphasize that a similar functional explanation could underlie other behavioural changes following territorial and/or aggressive encounters (such as winner/loser effects or changes in display frequency and territorial vigilance). Differences between my findings and those from previous studies suggest that the trade-off between antipredator behaviour and territorial defence can involve different costs from the trade-off between antipredator behaviour and foraging.     

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.     

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.       

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.     

Simulating winning in the wild — The behavioral and hormonal response of black redstarts to single and repeated territorial challenges of high and low intensity

In many vertebrates testosterone increases during aggressive interactions and the surges in this hormone may be responsible for the winner effect. So far studies on this relationship have been done in captivity only, because simulating a winning situation for a territory owner in the field is difficult. However, an increasing number of studies show that territorial aggression is not necessarily accompanied by elevated testosterone after a single simulated territorial intrusion (STI) and therefore it has been proposed that STIs may even create a losing experience. We examined whether free-living male black redstarts (Phoenicurus ochruros) show changes in androgens, corticosterone and behavior following repeated STIs of high or low intensity and in contrast to being challenged only once. Repeated intrusions had no influence on androgen and corticosterone levels regardless of intrusion intensity. In contrast, the behavioral response changed over days depending on the intensity of the intrusion. Only birds challenged with high-level intruders approached the decoy significantly faster during the third intrusion than during the first one, stayed closer to the decoy, and sang more songs than males challenged with low-level intruders. Thus, although black redstarts reacted differently to STIs varying in frequency and intensity, these behavioral differences were not reflected in androgen or corticosterone levels. Our data show that it is unlikely that STIs induce a losing experience. Furthermore, they indicate that a hormonal effect of winning an encounter may not be universal in vertebrates and may depend on the ecological or life-history context.     

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.     

A test of the dear enemy phenomenon in the Eurasian beaver

We tested the hypothesis that Eurasian beavers, Castor fiber, display the dear enemy phenomenon; that is, they respond less aggressively to intrusions by their territorial neighbours than to intrusions by nonterritorial floaters (strangers). This ability could be advantageous in facilitating differential treatment of wandering strangers versus established neighbours. Territorial beavers were presented with scent from neighbouring and stranger adult males. Thirty-nine different active beaver families, 18 in 1998 and 21 in 1999, were presented with a two-way choice between two pairs of experimental scent mounds; mounds with castoreum from a neighbour and a stranger, and mounds with anal gland secretion from a neighbour and a stranger. Direct observations of the families during evenings showed that: (1) beavers sniffed both castoreum and anal gland secretion from a stranger significantly longer than from a neighbour, and (2) beavers responded aggressively (stood on the mound on their hind feet, pawing and/or overmarking) significantly longer to castoreum, but not to anal gland secretion, from a stranger than from a neighbour. When experimental scent mounds were allowed to remain overnight and the beavers' responses were measured the following morning, the beavers' responses were significantly stronger to both castoreum and anal gland secretion from a stranger than from a neighbour. These findings indicate that Eurasian beavers can use scent to discriminate between neighbours and strangers, thereby supporting existence of the dear enemy phenomenon in this species. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

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.     

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.      

Simulating winning in the wild--the behavioral and hormonal response of black redstarts to single and repeated territorial challenges of high and low intensity

In many vertebrates testosterone increases during aggressive interactions and the surges in this hormone may be responsible for the winner effect. So far studies on this relationship have been done in captivity only, because simulating a winning situation for a territory owner in the field is difficult. However, an increasing number of studies show that territorial aggression is not necessarily accompanied by elevated testosterone after a single simulated territorial intrusion (STI) and therefore it has been proposed that STIs may even create a losing experience. We examined whether free-living male black redstarts (Phoenicurus ochruros) show changes in androgens, corticosterone and behavior following repeated STIs of high or low intensity and in contrast to being challenged only once. Repeated intrusions had no influence on androgen and corticosterone levels regardless of intrusion intensity. In contrast, the behavioral response changed over days depending on the intensity of the intrusion. Only birds challenged with high-level intruders approached the decoy significantly faster during the third intrusion than during the first one, stayed closer to the decoy, and sang more songs than males challenged with low-level intruders. Thus, although black redstarts reacted differently to STIs varying in frequency and intensity, these behavioral differences were not reflected in androgen or corticosterone levels. Our data show that it is unlikely that STIs induce a losing experience. Furthermore, they indicate that a hormonal effect of winning an encounter may not be universal in vertebrates and may depend on the ecological or life-history context.     

Differential effects of moving versus stationary territorial intruders on territory defence in a songbird

1.  In territorial contests, not only acoustic or other signals, but also the movements of a territorial intruder are likely to influence the response of a resident.
2.  We tested this movement hypothesis by simulating moving vs. stationary intruders into the territories of winter wrens Troglodytes troglodytes , using the same non-interactive song playbacks in both treatments.
3.  Male winter wrens showed a different long-term singing reaction in response to a moving than to a stationary intruder.
4.  One day after experiencing an intruder that was switching between three locations, residents started to sing earlier before sunrise, and they sang more and longer songs at dawn than before the intrusion.
5.  Residents receiving the same playback from one location only reacted by starting to sing later relative to sunrise, and by singing fewer and shorter songs than before the intrusion.
6.  We could not discriminate between the treatments when examining the short-term singing reactions during and immediately after the playbacks. However, our results clearly demonstrate an effect of the spatial behaviour of territorial intruders on the long-term territory defence of residents at dawn, about 24 h after an intrusion.
7.  We argue that spatial behaviour of territorial intruders should be an integral part of the study of animal territory defence behaviour. Investigating long-term changes in territory defence at dawn is a sensitive tool for discriminating between different types of intruders.     

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.     

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.     

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.     

鼹形田鼠入侵鼠和留居鼠之间的相互作用

我们研究了营掘地生活的社会性啮齿类——鼹形田鼠(Ellobius talpinus Pall．)对陌生鼠入侵完整家庭所占据洞穴系统后的行为和内分泌反应。在繁殖期和非繁殖期,所有的入侵鼠都在进入洞穴2天内从留居鼠的洞穴系统内消失;而在引入空洞穴的7只鼹形田鼠中,有4只至少在该洞穴中停留了2天。引入陌生鼠导致留居鼠在释放地的集中,并引起留居鼠和入侵鼠血浆中皮质酮水平的增加。在繁殖期,在引入陌生鼠的当天,也伴随着留居鼠血浆中睾酮增加的现象。所以,对陌生鼠入侵的模拟表明了留居鼹形田鼠有效的社会性防范,这可能是该物种家庭大小和结构稳定的一个重要机制。留居鼠和入侵鼠的相遇激活了压力的生理机制,特别是在繁殖季节更是如此[动物学报50(1)：19-26,2004]。     

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.     

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.     

Intra- and interspecific aggression do not modulate androgen levels in dusky gregories,yet male aggression is reduced by an androgen blocker

Discussions about social behavior are generally limited to fitness effects of interactions occurring between conspecifics. However, many fitness relevant interactions take place between individuals belonging to different species. Our detailed knowledge about the role of hormones in intraspecific interactions provides a starting point to investigate how far interspecific interactions are governed by the same physiological mechanisms. Here, we carried out standardized resident–intruder (sRI) tests in the laboratory to investigate the relationship between androgens and both intra- and interspecific aggression in a year-round territorial coral reef fish, the dusky gregory, Stegastes nigricans. This damselfish species fiercely defend cultivated algal crops, used as a food source, against a broad array of species, mainly food competitors, and thus represent an ideal model system for comparisons of intra-and interspecific territorial aggression. In a first experiment, resident S. nigricans showed elevated territorial aggression against intra- and interspecific intruders, yet neither elicited a significant increase in androgen levels. However, in a second experiment where we treated residents with flutamide, an androgen receptor blocker, males but not females showed decreased aggression, both towards intra- and interspecific intruders. Thus androgens appear to affect aggression in a broader territorial context where species identity of the intruder appears to play no role. This supports the idea that the same hormonal mechanism may be relevant in intra- and interspecific interactions. We further propose that in such a case, where physiological mechanisms of behavioral responses are found to be context dependent, interspecific territorial aggression should be considered a social behavior.     

Kinship,dear enemies,and costly combat: The effects of relatedness on territorial overlap and aggression in a cooperative breeder

Many species maintain territories, but the degree of overlap between territories and the level of aggression displayed in territorial conflicts can vary widely, even within species. Greater territorial overlap may occur when neighboring territory holders are close relatives. Animals may also differentiate neighbors from strangers, with more familiar neighbors eliciting less‐aggressive responses during territorial conflicts (the “dear enemy” effect). However, research is lacking in how both kinship and overlap affect territorial conflicts, especially in group‐living species. Here, we investigate kinship, territorial overlap, and territorial conflict in a habituated wild population of group‐living cooperatively breeding birds, the southern pied babbler Turdoides bicolor. We find that close kin neighbors are beneficial. Territories overlap more when neighboring groups are close kin, and these larger overlaps with kin confer larger territories (an effect not seen for overlaps with unrelated groups). Overall, territorial conflict is costly, causing significant decreases in body mass, but conflicts with kin are shorter than those conducted with nonkin. Conflicts with more familiar unrelated neighbors are also shorter, indicating these neighbors are “dear enemies.” However, kinship modulates the “dear enemy” effect; even when kin are encountered less frequently, kin elicit less‐aggressive responses, similar to the “dear enemy” effect. Kin selection appears to be a main influence on territorial behavior in this species. Groups derive kin‐selected benefits from decreased conflicts and maintain larger territories when overlapping with kin, though not when overlapping with nonkin. More generally, it is possible that kinship extends the “dear enemy” effect in animal societies.     

Interspecific Territoriality by a Rufous-Tailed Hummingbird (Amazilia tzacatl): Effects of Intruder Size and Resource Value1

I studied two aspects of interspecific territoriality in a Costa Rican nectarivorous bird, the rufous-tailed hummingbird (Amazilia tzacatl). First, I examined variation in the response of the territory holder to four species of intruding hummingbirds by quantifying the proportion of intruders chased from the territory. This measure of territory defense varied significantly among species of intruders and was negatively related to the intruding species’body mass, possibly due to potential costs associated with becoming involved in escalated contests with larger individuals. Second, I tested for an effect of resource manipulation on territory defense. I increased the resource value of the territory by injecting extant natural flowers with artificial sucrose solution. While the frequency of territorial intrusions did not change, the proportion of intruders chased by the territory holder increased. Apparently, nectar supplementation changed the territory holder's perception of resource value but had little impact on the intruders’perception.