Red Squirrels (Sciurus vulgaris) Respond to Alarm Calls of Eurasian Jays (Garrulus glandarius)

Recognition of heterospecific (interspecific) alarm calls has been demonstrated in birds and mammals, but bird–mammal interactions have rarely been studied. Here, I tested the hypothesis that red squirrels (Sciurus vulgaris) are able to recognize alarm calls of a sympatric bird species, the Eurasian jay (Garrulus glandarius), and respond adequately with anti‐predator behaviour. Both animals are preyed upon by the same predators. To test whether squirrels would react to heterospecific alarm calls, I recorded squirrels behaviour during playbacks of jay alarm calls, control playbacks (territorial songs of sympatric songbirds) and during silence. Differences between the control treatment (songbirds) and silence were not significant. Seven of the 13 squirrels responded with escape after broadcasting alarm calls of jays. Further, squirrels spent less time in the patch, expressed a higher vigilance, and showed more rapid head and body movements. These results suggest that squirrels recognize heterospecific alarm vocalizations of jays and discriminate them from equally loud non‐threatening sounds.     

The presence of an avian co-forager reduces vigilance in a cooperative mammal

Many animals must trade-off anti-predator vigilance with other behaviours. Some species facilitate predator detection by joining mixed-species foraging parties and ‘eavesdropping’ on the predator warnings given by other taxa. Such use of heterospecific warnings presumably reduces the likelihood of predation, but it is unclear whether it also provides wider benefits, by allowing individuals to reduce their own vigilance. We examine whether the presence of an avian co-forager, the fork-tailed drongo (Dicrurus adsimilis), affects rates of vigilance (including sentinel behaviour) in wild dwarf mongooses (Helogale parvula). We simulate the presence of drongos—using playbacks of their non-alarm vocalizations—to show that dwarf mongooses significantly reduce their rate of vigilance when foraging with this species. This is, to our knowledge, the first study to demonstrate experimentally that a mammal reduces vigilance in the presence of an avian co-forager.     

Florida Scrub-Jays (Aphelocoma coerulescens) are Sentinels More When Well-Fed (Even with no Kin Nearby)

Sentinels occupy high, exposed positions while other group members forage nearby. If sentinel behavior involves a foraging–predation risk trade‐off, animals should be sentinels more when fed supplemental food. When individual Florida scrub‐jays (Aphelocoma coerulescens) were fed fragments of peanuts, during the following 30 min they shifted 30% of their time from foraging to sentinel behavior. In a follow‐up experiment, we fed either one or two members in each group. As before, the jays reduced their foraging and spent much more time as sentinels when given supplemental food. In each treatment, pairs were sentinels simultaneously considerably less often than expected by chance. The dramatic shift from foraging to sentinel behavior suggests that for Florida scrub‐jays sentinel behavior brings substantial benefits for no greater cost than that of lost opportunities to forage. Because the results held for simple mated pairs of scrub‐jays, we argue that kin selection and social prestige are not necessary to explain sentinel behavior.     

Experimental evidence that sentinel behaviour is affected by risk

Sentinels are a conspicuous feature of some cooperative societies and are often assumed to provide benefits in terms of increased predator detection. Similar to other cooperative behaviours, variation in investment in sentinel behaviour should reflect variation in the benefits of such behaviour. However, evidence for this is inconclusive: to date experiments have manipulated the cost of sentinel behaviour, and considerations of changes in the benefits of sentinel activity on investment patterns are lacking. Here, we experimentally manipulated the benefits of sentinel behaviour in the cooperatively breeding pied babbler (Turdoides bicolor) to assess whether this had any impact on sentinel activity. We simulated the presence of an unseen predator using playbacks of heterospecific alarm calls, and the presence of an actual predator using a model snake. In both cases, the increase in perceived predation risk caused an increase in sentinel activity, demonstrating that investment in sentinel activity increases when the benefits are greater.     

Interspecific Semantic Alarm Call Recognition in the Solitary Sahamalaza Sportive Lemur,Lepilemur sahamalazensis

As alarm calls indicate the presence of predators, the correct interpretation of alarm calls, including those of other species, is essential for predator avoidance. Conversely, communication calls of other species might indicate the perceived absence of a predator and hence allow a reduction in vigilance. This “eavesdropping” was demonstrated in birds and mammals, including lemur species. Interspecific communication between taxonomic groups has so far been reported in some reptiles and mammals, including three primate species. So far, neither semantic nor interspecific communication has been tested in a solitary and nocturnal lemur species. The aim of this study was to investigate if the nocturnal and solitary Sahamalaza sportive lemur, Lepilemur sahamalazensis, is able to access semantic information of sympatric species. During the day, this species faces the risk of falling prey to aerial and terrestrial predators and therefore shows high levels of vigilance. We presented alarm calls of the crested coua, the Madagascar magpie-robin and aerial, terrestrial and agitation alarm calls of the blue-eyed black lemur to 19 individual Sahamalaza sportive lemurs resting in tree holes. Songs of both bird species’ and contact calls of the blue-eyed black lemur were used as a control. After alarm calls of crested coua, Madagascar magpie-robin and aerial alarm of the blue-eyed black lemur, the lemurs scanned up and their vigilance increased significantly. After presentation of terrestrial alarm and agitation calls of the blue-eyed black lemur, the animals did not show significant changes in scanning direction or in the duration of vigilance. Sportive lemur vigilance decreased after playbacks of songs of the bird species and contact calls of blue-eyed black lemurs. Our results indicate that the Sahamalaza sportive lemur is capable of using information on predator presence as well as predator type of different sympatric species, using their referential signals to detect predators early, and that the lemurs’ reactions are based on experience and learning.     

Nepotistic alarm calling in the Siberian jay, Perisoreus infaustus

From a life history perspective, parents have an incentive to protect their reproductive investment, and so may provide care even after their offspring are independent. Such prolonged parental care could lead to postponed dispersal of the offspring and thereby facilitate the formation of kin groups. We tested whether alpha birds in Siberian jays protected their independent, retained offspring by giving alarm calls during simulated predator attacks. We compared the responses to predator attacks simulated by flying a hawk model over a dyad of birds on a feeder for dyads composed of an alpha bird and either a relative or a nonrelative. Alpha females were nepotistic in their alarm-calling behaviour, in that they called more frequently when accompanied by their retained offspring than by unrelated immigrants, but alpha males called indiscriminately. This difference in alarm calling could reflect dominance relationships in Siberian jay groups, because the presence of immigrants may be less costly to alpha males, but alpha females are more vulnerable to competition from immigrants. Alarm calls were usually given during escape, when both individuals in the dyad had left the feeding site. However, results of a playback experiment suggest that alarm calls conveyed information about danger and incited an immediate escape reaction. Our results indicate that alarm calling can be nepotistic, and that factors other than kinship influence alarm-calling behaviour. Nepotistic antipredator behaviours are benefits that offspring can gain only in their natal territory. Hence, in the absence of preferential treatment by their parents, offspring may be more likely to disperse and kin groups are prevented from forming.     

Vigilance against predators induced by eavesdropping on heterospecific alarm calls in a non-vocal lizard Oplurus cuvieri cuvieri (Reptilia: Iguania)

Prey animals can reduce their risk of predation by detecting potential predators before encounters occur. Some animals gain information about nearby predators by eavesdropping on heterospecific alarm calls. Despite having well-developed ears, most lizards do not use vocal information for intraspecific communication, and few studies have shown practical use of the ears in wild lizards. Here, we show that the Madagascan spiny-tailed iguana (Oplurus cuvieri cuvieri) obtains auditory signals for predator detection. The Madagascan spiny-tailed iguana and the Madagascar paradise flycatcher (Terpsiphone mutata) are syntopic inhabitants of the Ampijoroa dry deciduous forest of Madagascar. The iguana and the flycatcher have neither a predator–prey relationship nor resource competition, but they have shared predators such as raptors and snakes. Using playback experiments, we demonstrated that the iguana discriminates mobbing alarm calls of the flycatcher from its songs and then enhances its vigilance behaviour. Our results demonstrate the occurrence of an asymmetrical ecological relationship between the Madagascan spiny-tailed iguana and the paradise flycatcher through eavesdropping on information about the presence of predators. This implies that indirect interspecific interactions through information recognition may be more common than generally thought in an animal community.     

Context-dependent group size choice in fish

The costs and benefits of group membership vary with the size of groups, and individuals are expected to modify their choice of groups in response to ecological factors such as food availability and predation risk. We experimentally examined context-dependent group size choice in a shoaling fish, the banded killifish, Fundulus diaphanus, by using nondirectional odour cues to simulate a food source or a successful attack by a predator (food or alarm treatments) in the laboratory. Group sizes were significantly smaller in the food treatment and larger in the alarm treatment than in control trials. When presented with food and alarm cues together, fish formed groups that were larger than control groups but smaller than those seen with alarm cues alone. These results are consistent with theoretical predictions based on the known benefits and costs of grouping and with previous laboratory work examining the individual shoal choice behaviour of single fish. To examine possible mechanisms of group formation, we developed an individual-based model of shoaling behaviour in which simulated fish were allowed to modify the area over which they interacted with neighbouring individuals. Group size distributions produced by the model were a good approximation of our experimental data. We suggest that local behavioural interaction rules of this type are a potential mechanism by which fish may individually adjust grouping behaviour without requiring extensive information on the position and movement of all possible shoalmates.     

The Predator Deterrence Function of Primate Alarm Calls

It is generally assumed that alarm calls function in intraspecific communication, for example to warn close relatives about the presence of a predator. However, an alternative hypothesis suggests that, in some cases, signallers may also gain fitness benefits in directly communicating to the predator, for example by advertising perception and unprofitability to predators that depend on unprepared prey. In this study, we show that six monkey species in Taï forest, Ivory Coast, produce significantly more alarm calls to leopards than to chimpanzees, although both are notorious monkey predators. The conspicuously high vocalization rates to leopards had adaptive consequences for the monkeys. By following a radio-collared leopard, we found that after detection and high alarm call rates the leopard gave up its hiding location and left the group significantly faster than would be expected by chance. We discuss these data with respect to the various functional hypothesis of alarm call behaviour and conclude that the high alarm call rates to leopards are part of an anti-predator strategy in primates that may have evolved to deter predators that depend on surprise.     

Does an opportunistic predator preferentially attack nonvigilant prey?

The dilution effect as an antipredation behaviour is the main theoretical reason for grouping in animals and states that all individuals in a group have an equal risk of being predated if equally spaced from each other and the predator. Stalking predators, however, increase their chance of attack success by preferentially targeting nonvigilant individuals, potentially making relative vigilance rates in a group relatively important in determining predation compared with the dilution effect. Many predators, however, attack opportunistically without stalking, when targeting of nonvigilant individuals may be less likely, so that the dilution effect will then be a relatively more important antipredation reason for grouping. We tested whether an opportunistically hunting predator, the sparrowhawk, Accipiter nisus, preferentially attacked vigilant or feeding prey models presented in pairs. We found that sparrowhawks attacked vigilant and feeding mounts at similar frequencies. Our results suggest that individuals should prioritize maximizing group size or individual vigilance dependent on the type of predator from which they are at risk. When the most likely predator is a stalker, individuals should aim to have the highest vigilance levels in a group, and there may be relatively little selective advantage to being in the largest group. In contrast, if the most likely predator is an opportunist, then individuals should simply aim to be in the largest group and can also spend more time foraging without compromising predation risk. For most natural systems this will mean a trade-off between the two strategies dependent on the frequency of attack of each predator type. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.     

Different Forms of Vigilance in Response to the Presence of Predators and Conspecifics in a Group-Living Mammal, the European Rabbit

In group‐living mammals, the major functions of vigilance are to detect the presence of predators and to monitor the movements of conspecific competitors, i.e. of potential opponents in agonistic encounters. The minimum distance to such a conspecific competitor that an animal considers safe is usually lower than to a predator, whereas the frequency of encounters with conspecifics is higher. Therefore, the acquisition of information about a predator or about a conspecific could lead to the existence of at least two different modes of vigilance behaviour. The aim of the present study was to describe and compare different forms of vigilance behaviour that European rabbits, Oryctolagus cuniculus, display in anti‐predator and social contexts. We conducted an observational study on individually marked animals from a field enclosure population. We recorded social interactions of the animals, the presence of aerial predators (common buzzard Buteo buteo), and the vigilance behaviour of the rabbits. We distinguished between two forms of vigilance of different intensity: subtle and overt. The frequencies of both forms of vigilance displayed by the rabbits differed significantly in occurrence, duration, and distribution over time. Females and males showed higher frequencies of overt but not subtle vigilance when buzzards were present. In contrast, the presence of conspecifics in close proximity affected the display of subtle but not overt vigilance: males increased the frequency of subtle vigilance when other males were close. Females increased subtle vigilance in proximity of males and females; however, this effect was only apparent in females with a more unstable social situation. In conclusion, European rabbits differentially increased two different forms of vigilance behaviour in social and anti‐predator contexts.     

Predator occurrence and perceived predation risk determine grouping behavior in guanaco (Lama guanicoe)

Grouping behavior of social ungulates may depend on both predator occurrence and perceived predation risk associated with habitat structure, reproductive state, and density of conspecifics. Over 3 years, we studied grouping behavior of guanaco (Lama guanicoe) families in Chilean Patagonia during the birthing season and determined their response to variation in predator occurrence and perceived predation risk (habitat structure, calf/adult rate, and density of conspecifics). We considered the effect of two predators, puma (Puma concolor) and culpeo fox (Lycalopex culpaeus). We measured two common (family group size and vigilance) and one novel (family group cohesion) behavioral responses of guanaco. Our results show that guanaco family groups adapted their grouping behavior to both predator occurrence and perceived predation risk. Larger family groups were found in open habitats and areas with high puma occurrence, while guanacos stayed in small family groups in areas with high shrub cover or low visibility. Group cohesion increased in areas with higher occurrence of pumas and culpeo foxes, and also increased in smaller family groups and in areas with low guanaco density. Vigilance (number of vigilant adults) was mainly related to group size and visibility, increasing in areas with low visibility, while residual vigilance (vigilance after removing the group‐size effect) did not vary with the explanatory variables examined. Our results suggest that a mix of predator occurrence and perceived predation risk influences guanaco grouping behavior and highlights the importance of evaluating different antipredator responses together and considering all predator species in studies aimed at understanding ungulate behavior.     

Vigilance in badgersMeles meles: the effects of group size and human persecution

Potential costs to badgersMeles meles (Linnaeus, 1758) of living in groups may be offset by the ability of a group to either improve predator detection, or reduce the time each individual must be vigilant to attain a certain likelihood of predator detection. Using an infra-red video-surveillance system, we show that badgers emerge later from their dens in a population that has been repeatedly subjected to lethal control by humans as compared to badgers from a nearby, undisturbed population. We further illustrate that, despite the apparent lack of a visual or vocal alarm signal to alert group members to a threat, corporate vigilance increases and individual vigilance levels decrease as badgers aggregate in groups (up to 4). These results highlight the possibility that the role of (human) predation in badger social evolution has not been sufficiently considered.     

Behavioural Responses of European Roe Deer to Temporal Variation in Predation Risk

In natural environments, predation risk varies over time. The risk allocation hypothesis predicts that prey is expected to adjust key anti‐predator behaviours such as vigilance to temporal variation in risk. We tested the predictions of the risk allocation hypothesis in a natural environment where both a species‐rich natural predator community and human hunters are abundant and where the differences in seasonal and circadian activity between natural and anthropogenic predators provided a unique opportunity to quantify the contributions of different predator classes to anti‐predator behaviour. Whereas natural predators were expected to show similar levels of activity throughout the seasons, hunter activity was high during the daytime during a clearly defined hunting season. According to the risk allocation hypothesis, vigilance should then be higher during the hunting season and during daytime hours than during the non‐hunting season and night‐time hours. Roe deer (Capreolus capreolus) on the edge of Bia?owie?a Primeval Forest in Eastern Poland displayed vigilance behaviour consistent with these predictions. The behavioural response of roe deer to temporarily varying predation risks emphasises the behavioural plasticity of this species and suggests that future studies of anti‐predator behaviour need to incorporate circadian variation in predation pressure as well as risk gradients of both natural and anthropogenic predators.     

Vigilance and Collective Detection of Predators in Degus (Octodon degus)

Individuals of social and partially social species typically reduce their vigilance activity when foraging in groups. As a result, per capita risk of predation decreases and individuals allocate more time to foraging and other fitness rewarding activities. Reduction of per capita risk is hypothesized to occur because there are more individuals to detect potential predators. If so, collective (i.e. total) vigilance is expected to increase with foraging group size. Increased surveillance during group foraging may occur if group members scan independently of one another, or sequentially to avoid the overlapping of their vigilance bouts. Intriguingly, such coordinated vigilance assumes that individuals monitor not only the presence, but the vigilance behaviour of group mates. We used seasonal records on time budget and grouping patterns of individually marked degus (Octodon degus), a social rodent, to examine if (a) individual vigilance decreases and/or foraging increases with group size, (b) collective vigilance increases with group size and (c) foraging degus coordinate their vigilance. When foraging, degus decreased their individual vigilance and increased their foraging time when in larger groups. Despite this, degus in larger groups increased their collective vigilance, supporting the hypothesis that socially foraging degus decrease predation risk through an improved ability to detect and escape potential predators. Additionally, patterns of collective vigilance suggested that degus scan independently of each other and so, they do not coordinate their vigilance to prevent its temporal overlapping. This finding does not support that foraging degus monitor the vigilance activity of group mates.     

The value of constant surveillance in a risky environment

In risky environments, where threats are unpredictable and the quality of information about threats is variable, all individuals face two fundamental challenges: balancing vigilance against other activities, and determining when to respond to warning signals. The solution to both is to obtain continuous estimates of background risk, enabling vigilance to be concentrated during the riskiest periods and informing about the likely cost of ignoring warnings. Human surveillance organizations routinely produce such estimates, frequently derived from indirect cues. Here we show that vigilant individuals in an animal society (the pied babbler, Turdoides bicolor) perform a similar role. We ask (i) whether, in the absence of direct predator threats, pied babbler sentinels react to indirect information associated with increased risk and whether they communicate this information to group mates; (ii) whether group mates use this information to adjust their own vigilance, and whether this influences foraging success; and (iii) whether information provided by sentinels reduces the likelihood of inappropriate responses to alarm calls. Using playback experiments, we show that: (i) sentinels reacted to indirect predator cues (in the form of heterospecific alarm calls) by giving graded surveillance calls; (ii) foragers adjusted their vigilance in reaction to changes in surveillance calls, with substantial effects on foraging success; and (iii) foragers reduced their probability of responding to alarm calls when surveillance calls indicated lowered risk. These results demonstrate that identifying attacks as they occur is only part of vigilance: equally important is continuous surveillance providing information necessary for individuals to make decisions about their own vigilance and evasive action. Moreover, they suggest that a major benefit of group living is not only the increased likelihood of detecting threats, but a marked improvement in the quality of information available to each individual.     

Influence of predation risk on the sheltering behaviour of the coral-dwelling damselfish, <Emphasis Type="Italic">Pomacentrus moluccensis</Emphasis>

Predation is a key ecosystem function, especially in high diversity systems such as coral reefs. Not only is predation one of the strongest top-down controls of prey population density, but it also is a strong driver of prey behaviour and function through non-lethal effects. We ask whether predation risk influences sheltering behaviour of damselfish living in mutualism with branching corals. Host corals gain multiple advantages from the mutualistic relationship which are determined by the strength of damselfish sheltering. Distance travelled by the Lemon Damselfish Pomacentrus moluccensis away from their host colony was measured here as a proxy for sheltering strength and was expected to be shortest under highest predation risk. Predation risk, defined as a function of predator abundance and activity, turbidity and habitat complexity, was quantified at four reef slope sites in Kepulauan Seribu, Indonesia. Damselfish sheltering strength was measured using stationary unmanned video cameras. Small damselfish (< 2 cm) increased their sheltering strength under high turbidity. Predator feeding activity, but not abundance, influenced damselfish sheltering strength. Contrary to our expectations, sheltering behaviour of adult damselfish decreased under high predator activity. While these observations are in line with risk-averse behaviour by juvenile P. moluccensis, they may indicate the presence of sentinel behaviour in the adults of this species. Habitat complexity seemed to be less important as a driver of damselfish behaviour. These counterintuitive results may indicate complex social behaviour and age-specific strategies for predator avoidance.     

Disturbances by dog barking increase vigilance in coots Fulica atra

Animals frequently interrupt their activity to look up and to scan their surrounding environment for potential predators (vigilance). As vigilance and other activities are often mutually exclusive, such behaviours are at the expense of feeding, sleeping or preening. Authors of many wildlife disturbance studies found that people with free-running dogs provoked the most pronounced disturbances (e.g. greater flushing distances and more birds affected). However, dogs on leash may also negatively affect wild animals, and barking dogs may lead to an increase in vigilance. In this study, I tested this hypothesis in coots (Fulica atra) using three different playback procedures: (1) dog barks, (2) conspecific coot alarm calls and (3) chaffinch song. The trials were conducted in spring and autumn 2005 at three study sites in southwestern Germany. During the dog playbacks, vigilance increased significantly from 17 to 28%. This increase in vigilance is comparable to the presence of a natural predator. As expected, vigilance also increased significantly during conspecific coot alarm calls but not during playbacks of the chaffinch song control. Two main findings result from the study: (1) coots respond to acoustic traits of dogs and may be able to acoustically recognise this predator and (2) this increase in vigilance might have implications for conservation, especially when considering buffer zones around sensitive areas.     

Nestling presence affects the anti-predator response of adult superb fairy-wrens (Malurus cyaneus)

Nest predation accounts for the majority of nesting failure, and hence there has been strong selection on behaviour to reduce nest predation, including patterns of nest defence. Here, we test risk-taking behaviour to experimentally placed predators in the presence or absence of nestlings. We use the superb fairy-wren (Malurus cyaneus) to test the prediction that vigilance will be comparable with and without nestlings, but that alarm vocalisations will increase when nestlings are present. We found support for both predictions. Adult vigilance of predators was comparable with and without nestlings. Alarm vocalisation intensity was predicted by predator type and nestling presence, and was highest to the snake model in the presence of nestlings. These results point to selection for differentiated nest defence response in relation to predator type and the presence or absence of nestlings.