Experimental evidence of specialised phenotypic roles in a mobbing raptor

Group living is associated with costs but also with potential benefits, such as a decrease in predation risk through, for example, higher defence efficiency. Mobbing is among the most specialised forms of anti-predator strategies involving group defence and has mainly been investigated in passerine birds and some mammals. Variation in the mobbing response has been found in several species according to phenotypic variation such as sex or age. This suggests that there are differential benefits between mobbers, which may have promoted individual specialisation in mobbing behaviour. We studied mobbing behaviour in a communal roosting raptor, the Marsh harrier (Circus aeruginosus), which shows active group defence. Our study population exhibits extreme colour polymorphism, with two colour morphs in males, as well as sexual dichromatism and colour variation with age. We used different decoys, placed at different distances from the roost, to manipulate experimentally the perceived predation risk and to elicit mobbing behaviour. Using the experimental design that maximised mobbing response in harriers, we then focused on the sequence and the specific behaviours involved in recruitment of mobbers, and whether individual investment in terms of defence was associated with phenotypic characteristics of individuals (i.e. sex, age and colour morph). We found that the main behaviour involved in successfully attracting mobbers was alarm calling. We also detected differential individual investment in relation to sex and age, but more importantly, we provide the first evidence for specialised male phenotypic roles during mobbing events, signalled by colour polymorphism: grey males tended not to be involved in mobbing and almost never behaved as recruiters or mobbers, while brown males behaved mainly as recruiter birds. These findings suggest that colour morph may signal the individual’s anti-predatory abilities through different behavioural strategies between males.     

Trading-off risks from predators and from aggressive hosts

Some birds exploit the aggressiveness of others that are more capable of defending their nests against predators. Usually this behaviour is selected for through improved breeding success for the timid (associate) species. The risk of predation from the more aggressive (host) species is generally rare but may select against the behaviour. The breeding success of red-breasted geese (Branta ruficollis) nesting in association with peregrine falcons (Falco peregrinus) in arctic Siberia was investigated from 1995 to 1999. Nest-predation risk for geese within colonies was positively correlated with distance from the falcons' eyries and negatively correlated with colony size. Though predation risk from the hosts was low, the risk of being attacked by the falcons was high, which we suggest explains why the likelihood of geese deserting their nests was negatively correlated with distance from the eyries. The optimal distance geese nested from eyries was 46 m, though only 37% of pairs managed to nest within 20 m of this. In years with low predation pressure, some geese within colonies nested farther from the falcons. This may be the first evidence to suggest a trade-off between costs and benefits in a nesting association, both of which are directly mediated by the host's nest defence behaviour.     

Interspecific attraction to the mobbing calls of black-capped chickadees (Parus atricapillus)

The species and number of birds attracted to playbacks of mobbing calls and song of the black-capped chickadee, Parus atricapillus, were compared. The chickadee vocalizations were played at abandoned chickadee nests, and the numbers and species of other birds that approached the speaker were tallied. Few non-chickadees were observed in the area when the song was played. That significantly more birds approached the speaker and displayed mobbing behavior during the mobbing call playback suggests that black-capped chickadee mobbing vocalizations carry meaning for at least ten other avian species. This finding supports the idea that species subjected to the same predators in an area may benefit by recognizing each others’ predator calls. This recognition may be facilitated by the similar structure of different species’ mobbing calls and also a learned association of another species’ call with the presence of a predator. Received: 23 March 1995 /Accepted after revision: 28 October 1995     

Snake-directed mobbing by the Formosan squirrel Callosciurus erythraeus thaiwanensis

Summary The Formosan squirrel Callosciurus erythraeus thaiwanensis was often observed mobbing the snake Elaphe climacophora. A total of 36 natural and 21 experimentally induced mobbings were observed and analyzed. The number of attending squirrels per mobbing event varied from one to seven, and 84% of observed mobbings were performed by more than one individual. The duration of a mobbing bout increased directly with the number of assembled mobbers. In 68% of cases, one adult female was one of the mobbers; there was never more than one female per mob. The number of assembled males per mob varied from 0 to 5; 40% of the mobbings involved two or more males. This difference is correlated to a difference in spacing patterns of both sexes; female home ranges were distributed exclusively, whereas male home ranges overlapped each other. Females mated with multiple males whose home ranges overlapped theirs. Female's reproductive status (conception, lactation, and weaning) affected their intensity of response to the playback of mobbing calls, females in pup-rearing period being the most sensitive. One function of the mobbing appears to be defense of the young against snake predation. Females mobbed more intensively and longer than males. Males that had resided at the study site for at least 1 year tended to mob more frequently than intruders.     

Risk assessment in western mosquitofish (Gambusia affinis): do multiple cues have additive effects?

The threat-sensitivity hypothesis predicts that prey individuals will increase antipredator behaviors as apparent predator risk increases. An implicit assumption of the threat-sensitivity hypothesis is that predator risk is additive. In other words, all characteristics of a predator that indicate risk should contribute in an additive way to determine the degree of risk-sensitive behavior. We tested this assumption in the laboratory by presenting live predators (green sunfish, Lepomis cyanellus) to groups of western mosquitofish (Gambusia affinis). We examined effects of predator diet, hunger level, and size on predator avoidance and inspection behavior of mosquitofish. Both predator diet and predator hunger level were significant and additive determinants of distance maintained from a predator, resulting in a graded response to combinations of these predator cues. In contrast, whereas predator diet was the most important determinant of general avoidance distances, predator hunger level was more important in determining mosquitofish vertical distribution and inspection behavior. Thus, the relationship between predator cue and the antipredator behavior that it elicits is dependent on which cues and behaviors are examined. Our data suggest that during risky behaviors, such as predator inspection, mosquitofish rely mainly on visual cues (behavior differences between hungry and satiated predators), whereas general avoidance behavior is determined by additive responses from visual and chemical cues.     

Predator-specific alarm calls in Campbell's monkeys, Cercopithecus campbelli

One of the most prominent behavioural features of many forest primates are the loud calls given by the adult males. Early observational studies repeatedly postulated that these calls function in intragroup spacing or intergroup avoidance. More recent field experiments with Diana monkeys (Cercopithecus diana) of Taï Forest, Ivory Coast, have clearly shown that loud male calls function as predator alarm calls because calls reliably (1) label different predator classes and (2) convey semantic information about the predator type present. Here, I test the alarm call hypothesis another primate, the Campbell's monkey (C. campbelli). Like Diana monkeys, male Campbell's monkeys produce conspicuous loud calls to crowned hawk eagles (Stephanoaetus coronatus) and leopards (Panthera pardus), two of their main predators. Playback experiments showed that monkeys responded to the predator category represented by the different playback stimuli, regardless of whether they consisted of (1) vocalisations of the actual predators (crowned hawk eagle shrieks or leopard growls), (2) alarm calls to crowned hawk eagles or leopards given by other male Campbell's monkeys or (3) alarm calls to crowned hawk eagles or leopards given by sympatric male Diana monkeys. These experiments provide further evidence that non-human primates have evolved the cognitive capacity to produce and respond to referential labels for external events.     

Threat-sensitive predator avoidance in damselfish-trumpetfish interactions

Summary Predatory threat can vary during a predator-prey interaction as an attack escalates or among predators at different times. A Threat-sensitivity hypothesis is presented which predicts that prey individuals will trade-off predator avoidance against other activities by altering their avoidance responses in a manner that reflects the magnitude of the predatory threat. This hypothesis was tested in the field by presenting prey (threespot damselfish, Stegastes planifrons) with models of foraging predators (Atlantic trumpetfish, Aulostomus maculatus). During a presentation, damselfish displayed progressively stronger avoidance as predator models were brought nearer; response waned rapidly once predator models passed overhead. Larger predator models and those oriented in a strike pose evoked stronger avoidance reactions than smaller and non-attacking models, intermediate responses were evoked by size and orientation combinations that were intermediate in threat, and habituation was more common to weakly-threatening presentations. Smaller damselfish showed stronger avoidance of models than did larger damselfish. Nonavoidance activities, such as feeding and territorial defense, were curtailed during presentations or were more common during weakly threatening presentations. Approaches to the models, equated with mobbing, were more common among large damselfish, again reflecting degrees of vulnerability among different size prey individuals. These initial results indicate that damselfish threatened by predators respond in a graded manner that reflects the degree of threat posed by the predator, in accordance with the Threat-sensitivity hypothesis.     

The paradox of risk assessment: comparing responses of fathead minnows to capture-released and diet-released alarm cues from two different predators

Summary. Many aquatic prey are known to use chemical alarm cues to assess their risk of predation. In fishes, such alarm cues can be released either through damage of the epidermis during a predatory attack (capture-released) or through release from the predator feces (diet-released). In our study, we compared the importance of capture- versus diet-released alarm cues in risk assessment by fathead minnows (Pimephales promelas) that were na?ve to fish predators. We utilized two different fish predators: a specialized piscivore, the northern pike (Esox lucius) and a generalist predator, the brook trout (Salvelinus fontinalis). Handling time of pike consuming minnows was much shorter than for trout consuming minnows, likely resulting in less epidermal damage to the minnows during attacks by pike. In accordance with this, minnows showed a less intense antipredator response to capture-released cues from pike than capture-released cues from trout. This represents a paradox in risk assessment for the minnows as they respond to the specialized piscivore, the more dangerous predator, with a less intense antipredator response. In contrast, the minnows showed a stronger antipredator response to the specialized piscivore than to the generalist when given diet cues. This work highlights the need for researchers to carefully consider the nature of the information available to prey in risk assessment.     

Ontogenetic differences in chemical alarm cue production determine antipredator responses and learned predator recognition

How individuals assess, respond and subsequently learn from alarm cues is crucial to their survival and future fitness. Yet this information is not constant through time; many individuals are exposed to different predators throughout their life as they outgrow some predators or move to habitats containing different predators. To maximise overall fitness, individuals should discriminate between different cues and respond and learn from only those that are relevant to their current ontogenetic stage. We tested whether juvenile spiny chromis, Acanthochromis polyacanthus, could distinguish between chemical alarm cues from conspecific donors of different ontogenetic stages and whether the cue ontogenetic stage of the cue donor affected the efficacy of learning about predators. Juveniles displayed a significant antipredator response when conditioned with juvenile chemical alarm cues paired with predator odour but failed to respond when conditioned with predator odour paired with either adult alarm cues or with saltwater. Subsequently, individuals only recognised the predator odour alone as a threat when conditioned with juvenile alarm cues. This demonstrates that prey may be highly specific in how they use information from conspecific alarm cues, selectively responding to and learning from only those cues that are relevant to their developmental stage.     

Group-living in cliff swallows as an advantage in avoiding predators

Summary Cliff swallows (Hirundo pyrrhonota) in SW Nebraska, USA, nest in colonies and associate in groups away from their colonies. The degree to which group-living in this species affords advantages in the avoiding of predators was examined. The distance from the colony at which a snake predator was detected increased with colony size. In flocks away from the colonies, group vigilance increased, but the time that each individual spent vigilant decreased, with flock size. As a result, birds in large flocks had more time for preening and mud-gathering. Cliff swallows did not effectively mob predators and thus were unable to deter predators regardless of group size. Nesting within each colony was highly synchronous, but when the effects of ectoparasites on nesting success were removed, individuals nesting during the peak breeding period were no more successful than those nesting before or after the peak. This suggests that swamping of predators is unlikely in cliff swallow colonies. Nests at the edges of colonies were more likely to be preyed upon than nests nearer the center, suggesting that colonial nesting conferred some selfish herd benefits. Overall reproductive success did not vary with colony size. While cliff swallows receive some anti-predator benefits by living in groups, the avoidance of predators is probably not a major selective force for the evolution of coloniality in this species.     

Differential predator escape performance contributes to a latitudinal sex ratio cline in a migratory shorebird

Sexual segregation outside the mating season is common in vertebrates, and has been attributed to sexual differences in predator escape performance in ungulates and fish, but not in birds. Here, we tested the hypothesis that sex- and latitude-specific predator escape performance underlies the differential nonbreeding distribution of western sandpipers (Calidris mauri), a migratory shorebird. Females overwinter further south along the American Pacific coast, creating a latitudinal cline in sex ratio. Escape performance is reduced with increasing body mass, and birds generally carry less fat further south. Western sandpipers with poor escape performance were therefore predicted to prefer southern sites to reduce the risk of mortality posed by predators. Data from four nonbreeding latitudes showed that wing loading, used as an index of escape performance, was overall higher for females, and that it decreased with latitude in both sexes. Within latitudes, wing loading was lower at smaller, and presumably more dangerous, sites. Flight response to a predatory attack was longer in the south. Mortality risk offers a novel and candidate explanation for differential distribution patterns in western sandpipers and possibly other avian migrants.     

Experimental evidence of reciprocal altruism in the pied flycatcher

Although human behaviour abounds with reciprocal altruism, few examples exist documenting reciprocal altruism in animals. Recent non-experimental evidence suggests that reciprocal altruism may be more common in nature than previously documented. Here we present experimental evidence of mobbing behaviour, the joint assault on a predator in an attempt to drive it away, as reciprocal altruism in the breeding pied flycatcher (Ficedula hypoleuca). Given a choice, pied flycatchers assisted in mobbing initiated by co-operating neighbours and did not join in mobbing when initiated by conspecific neighbours which had defected from necessary assistance 1 h before. The results suggest the birds followed a ‘tit-for-tat’-like strategy and that mobbing behaviour of breeding birds may be explained in terms of reciprocal altruism.     

Determinants of brood defence in the great tit Parus major L.

Summary Great tits (Parus major) tending nestlings reacted defensively to a live predator (Glaucidium perlatum; domestic cat) and the playback of a mixed species mobbing chorus, or to the latter alone. Defensive behaviour, mainly mobbing, reflected the risk taken and is assessed by five measures. Multivariate and contingency analyses revealed that at least 11 of 16 contextual independent variables affected the risk taken. Incremental effects are due to: Age of young, sex of the defending bird, the expected number of neighbouring mobbers, low temperature, wet canopy, the raptor's distance from cover, coniferous forest, advancing season. A decremental effect is exerted by a large brood that is older. Annual differences in defence arise probably from demographic factors such as fecundity, which in turn affect the parent's benefit-cost ratio (number of young of the same sex as the parent/residual reproductive value of the parent).While the effects of annual fecundity, age of young and season were predicted on the basis of this benefit-cost ratio, the failure to verify an incremental effect of brood size runs counter to established theory. We conclude that parents gear their defence efforts to energy investment, past or future, and are mal-adapted to brood size as a promotor of risk taken. The influence of the habitat is poorly understood. At least three factors (age and number of young, parent's sex) act additively on part of the response. Despite the large number of variables examined, about 43% of the total response variance remains unexplained.While four defence measures are determined by at least 10 contextual factors, a fifth measure, the male's minimum distance from the raptor, is determined by one other factor, the appearance of the male. The latter leads us to assume an additional, social rôle of brood defence.Risk-assessment by great tits leading to risk-aversive defence behaviour is governed by evolved restraints rather than by momentary constraints. Examples are provided by the effects of weather and cover.     

Individual differences in nest defense in the colonial breeding Black-tailed Gulls

Often in colonial seabirds, all colony members are believed to defend against nest predators and experience equal nest predation risk. However, the variation of defense behavior among members and its reproductive consequences are largely unknown. We investigated (1) individual variation in the nest defense of breeding Black-tailed Gulls Larus crassirostris against a natural egg predator, the Jungle Crow Corvus macrorhynchos and (2) how this behavioral variation affects an individual’s own nest predation risk and that of their neighbors. Results were compared between 2 years where crow attack levels were manipulated to average 5 and 22 times normal rates (“low” and “high” predation risk years, respectively) by the placement of varying numbers of artificial nests containing unguarded eggs at the perimeter of the gull colony. In both years, 23–38% of parents, mostly males, showed “aggressive” defense behavior (strikes or chases) against crows and decoys. Other “non-aggressive” gulls showed no defense. In the year of low predation risk, intrusion rates by crows (landing within 0.5 m of an individual gull’s nest) were similar for aggressive and non-aggressive gulls. In the year of high predation risk, however, the rates of intrusion for aggressive gulls (4%) and for non-aggressive gulls with an aggressive neighbor (37%) were significantly lower than for non-aggressive gulls without an aggressive neighbor (76%). These results indicate that aggressive individuals reduce nest predation risk for themselves and conspecific neighbors in a colonially breeding species.     

The spider and fly revisited: ploy–counterploy behavior in a unique predator–prey system

Earlier studies have shown that the sarcophagid fly Arachnidomyia lindae is the principal egg-sac predator of the colonial orb-weaving spider Metepeira incrassata, and that risk of egg-sac loss increases with group size. Observations of specialized behaviors for attack (flies) and defense (spiders) suggest that this predator-prey relationship may incorporate elements of ploy and counterploy behavior. Here we explore this relationship in detail and test hypotheses regarding efficacy of attack and defense behaviors. Egg-sac guarding by the spider includes defensive behaviors specific to this fly predator, which were observed during experimental "attacks" with tethered A. lindae, but not with similar presentations of non-predatory Musca domestica. Experimental studies also show that Metepeira incrassata recognizes this predatory fly by airborne cues (i.e., the signature frequency of wing-beats), and can distinguish between this predator and other flies (potential prey) on the basis of wing-beat frequency differences. Removal of female spiders results in a significantly higher probability of unguarded egg-sacs being parasitized, demonstrating the adaptive value of spider defensive behaviors. We also present evidence that A. lindae utilizes a behavioral ploy for circumventing spider guarding behavior (aggressive mimicry - producing vibrations of captured prey in the web), and that Metepeira incrassata, in turn, exhibits a counter-ploy behavior (signal thread cutting) to eliminate this potentially distracting vibratory information. While previous studies have shown that this colonial web-building spider uses a number of general attack-abatement mechanisms against a diversity of predators and parasitoids, results of this study suggest that selection pressures from a highly specialized predator may also result in evolution of predator-specific prey responses.     

Does responsiveness to predator scents affect lizard survivorship?

Many prey organisms respond to predator scent by shifting behaviour. These alterations to behaviour are often assumed to increase an animal's chances of evading predators. Responsiveness to predator scents is therefore believed to ultimately increase a prey's chances of surviving encounters with predators. This notion is widely accepted among behavioural ecologists but has rarely been empirically tested. I staged encounters between adult snakes (Demansia psammophis) and pairs of unrestrained adult lizards (Lampropholis guichenoti) that responded strongly to snake predator scent ("responsive") or weakly to snake predator scent ("non-responsive"). Responsive lizards decreased activity and mobility during the staged encounters with snake predators. In turn this shift in behaviour decreased the chances that snakes detected responsive lizards. Since snakes almost always captured lizards that were detected, responding strongly to predator scent decreased a lizard's chances of being captured by predators. This finding is the first experimental demonstration in any terrestrial animal that responsiveness to predator scents can function to increase survival probability.     

Does reproductive state affect a lizard's behavior toward predator chemical cues?

We examined how reproductive state affected shifts in behavior of adult female Podarcis sicula toward chemical cues from a natural snake predator (Coronella austriaca). The oviparous P. sicula lizards do not experience a major physical burden during reproduction, but gravid females substantially increase duration of basking. Therefore, gravid lizards are likely to experience a greater risk of mortality because they are exposed to predators for longer periods. Both gravid and non-gravid females shifted patterns of locomotion when confronted with snake chemical cues, but the change was notably larger when females were non-gravid. When non-gravid, lizards responded to predator scent by increasing the number of stand-ups and starts, while such a response was not observed when females were gravid. By contrast, gravid lizards clearly reduced the time spent basking in the presence of predator scent, whereas no change in basking behavior was observed when females were non-gravid. Thus, females exhibit differential behavioral responses to predator scents that is dependent on reproductive state.     

Anti-predator benefits of group living in white-nosed coatis (Nasua narica)

Predation is often considered an important factor in the evolution of sociality among animals. We studied mortality patterns and grouping behavior of white-nosed coatis (Nasua narica) at sites in southern Arizona, USA, and western Jalisco, México. Coatis were monitored by radio-tracking and recaptures for more than 3 years at each site. In both populations, predation by large felids, including jaguars (Panthera onca) and pumas (Puma concolor), accounted for more than 50% of mortality of adult coatis. Predation rates were significantly higher on solo coatis than on coatis in groups at both study sites. Predation rates were negatively related to group size in Arizona. However, mortality of juveniles, as measured by the ratios of juveniles to adult females, was not related to the number of adult females per group in Arizona or Jalisco. Coatis exhibit a suite of behaviors, including foraging with the juveniles in the center of the group, sharing vigilance, alarm calling, mobbing and attacking predators, and a highly synchronous birth season, that are all consistent with the hypothesis that predation has played an important role in shaping coati social behavior.     

Kill before being killed: an experimental approach supports the predator-removal hypothesis as a determinant of intraguild predation in top predators

Intraguild predation (IGP) has been explained in terms of competitor-removal, food-stress and predator-removal hypotheses. Only the first two hypotheses have been fairly well studied. To test the predator-removal hypothesis as a force determining IGP in avian predators, we performed a field experiment to simulate the presence of an IG predator (eagle owl Bubo bubo dummy) in the surrounding of the nests of four potential IG prey (black kite Milvus migrans, red kite Milvus milvus, booted eagle Aquila pennata and common buzzard Buteo buteo). To discard the possibility that an aggressive reaction towards the eagle owl was not related to the presence of the IG predator, we also presented a stuffed tawny owl Strix aluco, which is a potential competitor but cannot be considered an IG predator of the studied diurnal raptors considered in the experiment. While almost always ignoring the tawny owl, raptors chiefly showed an interspecific aggressive behaviour towards their IG predator. Our results seem to support the predator-removal hypothesis, as the IG prey may take advantage of the diurnal inactivity of the IG predator to remove it from their territory. However, the recorded behaviour may be also considered as a special variety of mobbing (i.e. a prey’s counter-strategy against its predator), where the mobber is sufficiently powerful to escalate predator harassment into deliberate killing attempts. In their turn, eagle owls can respond with an IG predatory behaviour aimed at removing IG prey species which are highly aggressive mobbers.     

Linking edge effects and patch size effects: Importance of matrix nest predators

The edge effect is usually considered to be the proximate cause of area sensitivity in forest birds. We tested if birds nesting in large patches are less vulnerable to the edge effect using a simple model that assumes an increase in patch size reduces the probability of a matrix predator moving to the core areas of forest and that larger perimeter/area ratios result in a higher number of matrix predators per unit of area. The probability of a nest being successful decreased asymptotically with an increase in either the patch penetration distance of predators or predator density, but those effects were reduced when patch size was increased. Large patches have a lower probability of being affected by an Allee effect and they can function as sink habitats only if penetration distance and predator density are largely increased. However, the transition from an Allee effect to a sink condition occurs with a small increase in penetration distance and predator density. Since birds nesting in large patches are less vulnerable to an increase in matrix predator populations, persistence of bird populations may be possible by increasing the size of habitat patches that can act as source populations.