Referential calls signal predator behavior in a group-living bird species

Predation is a powerful agent of natural selection, driving the evolution of antipredator calls [1]. These calls have been shown to communicate predator category [2-4] and/or predator distance to conspecifics [5-7]. However, the risk posed by predators depends also on predator behavior [8], and the ability of prey to communicate predator behavior to conspecifics would be a selective advantage reducing their predation risk. I tested this idea in Siberian jays (Perisoreus infaustus), a group-living bird species. Predation by hawks, and to a lesser extent by owls, is substantial and the sole cause of mortality in adult jays [9]. By using field data and predator-exposure experiments, I show here that jays used antipredator calls for hawks depending on predator behavior. A playback experiment demonstrated that these prey-to-prey calls were specific to hawk behavior (perch, prey search, attack) and elicited distinct, situation-specific escape responses. This is the first study to demonstrate that prey signals convey information about predator behavior to conspecifics. Given that antipredator calls in jays aim at protecting kin group members [10, 11], consequently lowering their mortality [9], kin-selected benefits could be an important factor for the evolution of predator-behavior-specific antipredator calls in such systems.     

Mobbing calls signal predator category in a kin group-living bird species

Many prey species gather together to approach and harass their predators despite the associated risks. While mobbing, prey usually utter calls and previous experiments have demonstrated that mobbing calls can convey information about risk to conspecifics. However, the risk posed by predators also differs between predator categories. The ability to communicate predator category would be adaptive because it would allow other mobbers to adjust their risk taking. I tested this idea in Siberian jays Perisoreus infaustus, a group-living bird species, by exposing jay groups to mounts of three hawk and three owl species of varying risks. Groups immediately approached to mob the mount and uttered up to 14 different call types. Jays gave more calls when mobbing a more dangerous predator and when in the presence of kin. Five call types were predator-category-specific and jays uttered two hawk-specific and three owl-specific call types. Thus, this is one of the first studies to demonstrate that mobbing calls can simultaneously encode information about both predator category and the risk posed by a predator. Since antipredator calls of Siberian jays are known to specifically aim at reducing the risk to relatives, kin-based sociality could be an important factor in facilitating the evolution of predator-category-specific mobbing calls.     

Do anuran larvae respond behaviourally to chemical cues from an invasive crayfish predator? A community-wide study

Antipredator behaviour is an important fitness component in most animals. A co-evolutionary history between predator and prey is important for prey to respond adaptively to predation threats. When non-native predator species invade new areas, native prey may not recognise them or may lack effective antipredator defences. However, responses to novel predators can be facilitated by chemical cues from the predators’ diet. The red swamp crayfish Procambarus clarkii is a widespread invasive predator in the Southwest of the Iberian Peninsula, where it preys upon native anuran tadpoles. In a laboratory experiment we studied behavioural antipredator defences (alterations in activity level and spatial avoidance of predator) of nine anurans in response to P. clarkii chemical cues, and compared them with the defences towards a native predator, the larval dragonfly Aeshna sp. To investigate how chemical cues from consumed conspecifics shape the responses, we raised tadpoles with either a tadpole-fed or starved crayfish, or dragonfly larva, or in the absence of a predator. Five species significantly altered their behaviour in the presence of crayfish, and this was largely mediated by chemical cues from consumed conspecifics. In the presence of dragonflies, most species exhibited behavioural defences and often these did not require the presence of cues from predation events. Responding to cues from consumed conspecifics seems to be a critical factor in facilitating certain behavioural responses to novel exotic predators. This finding can be useful for predicting antipredator responses to invasive predators and help directing conservation efforts to the species at highest risk.     

Do Naïve Primates Recognize the Vocalizations of Felid Predators?

Traits that were adaptive under previous conditions may no longer have fitness benefits. However, some species still retain appropriate antipredator behaviors even though they do not coexist with the predators that their ancestors once faced. Studies have examined the responses of a variety of naïve species to these predators, but none have specifically investigated whether naïve primates retain antipredator behaviors against felid predators. We studied the pig‐tailed langur (Simias concolor) to determine whether it still recognizes felids as predators even though dangerous felids do not exist on the islands on which it inhabits. The responses of the langurs to the playbacks of the vocalizations of felids (an ancestral predator), elephants (an unknown animal but not a predator), humans (a known predator) and, pigs and birds (known animals but not predators) were compared. Langurs fled more slowly and looked at the speaker less in response to the felid and elephant calls than they did in response to the human voices. Similar numbers of langurs fled in response to all playback treatments except the pig and bird. The results suggest that langurs are afraid of novel vocalizations but have not retained specific acoustic knowledge of felid predator vocalizations. For long‐lived species that have extended periods of learning, being able to modify general behavioral responses, such as antipredator behaviors, based on individual experiences may be more adaptive than having fixed behavioral strategies.     

Observational and Experimental Evidence for the Function of Tail Flicking in Eurasian Moorhen Gallinula chloropus

Tail movements such as wagging, flicking or pumping are reported from many bird species but their adaptive functions remain poorly understood. To investigate whether tail flicking functions as an alarm signal, either to predators or neighbouring birds, or as a signal of submission to conspecifics, I observed this behaviour in moorhen in a natural context, and conducted playback experiments using vocalizations of predators, conspecifics and heterospecifics. I found positive relationships between flicking and vigilance and nearest neighbour distance, and negative relationships between flicking and moorhen flock size and total flock size. Moorhen at the edge of a flock flicked at a higher rate. Single moorhen flicked more often compared with individuals in groups, both in single‐ and mixed‐species flocks, and there was a tendency that single moorhen flicked more often than single moorhen within a mixed‐species flock. Moorhen responded differently to conspecific and predator calls. While in both cases vigilance increased, tail flick rate was higher during predator playbacks and lower during conspecific playbacks. Furthermore, moorhen remained rather motionless when conspecific calls were played back, but not during predator calls, and, moorhen resumed to a baseline level of tail flicking more quickly after the playback of conspecific calls. Taken together, the results suggest that flicking may be considered as a honest signal of vigilance directed towards ambushing predators.     

Behavioral responses to conspecific mobbing calls are predator‐specific in great tits (Parus major)

When facing a predator, animals need to perform an appropriate antipredator behavior such as escaping or mobbing to prevent predation. Many bird species exhibit distinct mobbing behaviors and vocalizations once a predator has been detected. In some species, mobbing calls transmit information about predator type, size, and threat, which can be assessed by conspecifics. We recently found that great tits (Parus major) produce longer D calls with more elements and longer intervals between elements when confronted with a sparrowhawk, a high‐threat predator, in comparison to calls produced in front of a less‐threatening tawny owl. In the present study, we conducted a playback experiment to investigate if these differences in mobbing calls elicit different behavioral responses in adult great tits. We found tits to have a longer latency time and to keep a greater distance to the speaker when sparrowhawk mobbing calls were broadcast. This suggests that tits are capable of decoding information about predator threat in conspecific mobbing calls. We further found a tendency for males to approach faster and closer than females, which indicates that males are willing to take higher risks in a mobbing context than females.     

Heterospecific recognition of referential alarm calls in two species of lemur

ABSTRACT

Alarm vocalizations are a common feature of the mammalian antipredator response. The meaning and function of these calls vary between species, with some species using calls to reference-specific categories of predators. Species can also use more than just the calls of conspecifics to detect threat, ‘eavesdropping’ on other species’ signalling to avoid predation. However, the evidence to date for both referential signalling and eavesdropping within primates is limited. We investigated two sympatric populations of wild lemur, the Coquerel’s sifaka Propithecus coquereli and the common brown lemur Eulemur fulvus, presenting them with playbacks of predator calls, conspecific alarm calls and heterospecific lemur alarm calls, and recorded their behavioural responses following the playbacks. Results suggest that the Coquerel’s sifaka may have functionally referential alarm calls with high specificity for aerial predators, but there was no evidence for any referential nature of the other call investigated. Brown lemurs appear to have a mixed alarm system, with one call being specific with respect to aerial predators. The other call investigated appeared to reference terrestrial predators. However, it was also used in other contexts, so does not meet the criteria for functional reference. Both species showed evidence for heterospecific alarm call recognition, with both the Coquerel’s sifaka and the brown lemurs responding appropriately to heterospecific aerial alarm calls.     

On the Meaning of Alarm Calls: A Review of Functional Reference in Avian Alarm Calling

A long‐standing question in animal communication is whether signals reveal intrinsic properties of the signaller or extrinsic properties of its environment. Alarm calls, one of the most conspicuous components of antipredator behaviour, intuitively would appear to reflect internal states of the signaller. Pioneering research in primates and fowl, however, demonstrated that signallers may produce unique alarm calls during encounters with different types of predators, suggesting that signallers through selective production of alarm calls provide to conspecific receivers information about predators in the environment. In this article, we review evidence for such ‘functional reference’ in the alarm calls of birds based on explicit tests of two criteria proposed in Macedonia & Evans’ (Ethology 93, 1993, 177) influential conceptual framework: (1) that unique alarm calls are given to specific predator categories, and (2) that alarm calls isolated from contextual information elicit antipredator responses from receivers similar to those produced during actual predator encounters. Despite the importance of research on birds in development of the conceptual framework and the ubiquity of alarm calls in birds, evidence for functionally referential alarm calls in this clade is limited to six species. In these species, alarm calls are associated with the type of predator encountered as well as variation in hunting behaviour; with defence of reproductive effort in addition to predators of adults; with age‐related changes in predation risk; and with strong fitness benefits. Our review likely underestimates the occurrence of functional reference in avian alarm calls, as incomplete application and testing of the conceptual framework has limited our understanding. Throughout, therefore, we suggest avian taxa for future studies, as well as additional questions and experimental approaches that would strengthen our understanding of the meaning of functional reference in avian alarm calls.     

Responses to terrestrial nest predators by endemic and introduced Hawaiian birds

Birds free from nest predators for long periods may either lose the ability to recognize and respond to predators or retain antipredator responses if they are not too costly. How these alternate scenarios play out has rarely been investigated in an avian community whose members have different evolutionary histories. We presented models of two nest predators (rat and snake) and a negative control (tree branch) to birds on Hawai?i Island. Endemic Hawaiian birds evolved in the absence of terrestrial predators until rats were introduced approximately 1,000 years ago. Introduced birds evolved with diverse predator communities including mammals and snakes, but since their introduction onto the island approximately one century ago have been free from snake predation. We found that (a) endemic and introduced birds had higher agitation scores toward the rat model compared with the branch, and (b) none of the endemic birds reacted to the snake model, while one introduced bird, the Red‐billed Leiothrix (Leiothrix lutea), reacted as strongly to the snake as to the rat. Overall, endemic and introduced birds differ in their response to predators, but some endemic birds have the capacity to recognize and respond to introduced rats, and one introduced bird species retained recognition of snake predators from which they had been free for nearly a century, while another apparently lost that ability. Our results indicate that the retention or loss of predator recognition by introduced and endemic island birds is variable, shaped by each species' unique history, ecology, and the potential interplay of genetic drift, and that endemic Hawaiian birds could be especially vulnerable to introduced snake predators.     

Avoiding predators at night: antipredator strategies in red-tailed sportive lemurs (Lepilemur ruficaudatus)

Although about one-third of all primate species are nocturnal, their antipredator behavior has rarely been studied directly. Crypsis and a solitary lifestyle have traditionally been considered to be the main adaptive antipredator strategies of nocturnal primates. However, a number of recent studies have revealed that nocturnal primates are not as cryptic and solitary as previously suggested. Thus, the antipredator strategies available for diurnal primates that rely on early detection and warning of approaching predators may also be available to nocturnal species. In order to shed additional light on the antipredator strategies of nocturnal primates, I studied pair-living red-tailed sportive lemurs (Lepilemur ruficaudatus) in Western Madagascar. In an experimental field study I exposed adult sportive lemurs that lived in pairs and had offspring to playbacks of vocalizations of their main aerial and terrestrial predators, as well as to their own mobbing calls (barks) given in response to disturbances at their tree holes. I documented the subjects' immediate behavioral responses, including alarm calls, during the first minute following a playback. The sportive lemurs did not give alarm calls in response to predator call playbacks or to playbacks with barks. Other behavioral responses, such as gaze and escape directions, corresponded to the hunting strategies of the two classes of predators, suggesting that the corresponding vocalizations were correctly categorized. In response to barks, they scanned the ground and fled. Because barks do not indicate any specific threats, they are presumably general alarm calls. Thus, sportive lemurs do not rely on early warning of acoustically simulated predators; rather, they show adaptive escape strategies and use general alarm calls that are primarily directed toward the predator but may also serve to warn kin and pair-partners.     

No evidence of eavesdropping on heterospecific alarm calls by captive zebra finches recently descended from wild birds

Alarm calls are vocalisations animals give in response to predators which mainly function to alert conspecifics of danger. Studies show that numerous species eavesdrop on heterospecific calls to gain information about predator presence. Responding to heterospecific calls may be a learned or innate response, determined by whether the response occurs with or without prior exposure to the call. In this study, we investigated the presence of eavesdropping behaviour in zebra finches Taeniopygia guttata. This species is not known to possess a distinct alarm call to warn adult conspecifics of a threat, and could be relying on alarm calls of nearby heterospecifics for predator information. We used a playback experiment to expose captive zebra finches to three heterospecific sounds: an unfamiliar alarm call (from the chestnut‐rumped thornbill Acanthiza uropygialis), a familiar alarm call, and a familiar control (both from the noisy miner Manorina melanocephala). These calls were chosen to test if the birds had learnt to distinguish between the function of the two familiar calls, and if the acoustic properties of the unfamiliar alarm indicated presence of a threat to the finches. Our results showed that in response to the thornbill alarm, the birds reduced the rate of production of short calls. However, this decrease was also seen when considering both short and distance calls in response to the control sound. An increase in latency to call was also seen after the control stimulus when compared to the miner alarm. The time spent scanning increased in response to all three stimuli, but this did not differ between stimuli. There were no significant differences when considering the stimulus by time interaction for any of the three vigilance measures. Overall, no strong evidence was found to indicate that the captive zebra finches were responding to the heterospecific alarm stimuli with anti‐predator behaviour.     

The biological function of gulls' attraction towards predators

Many species of birds and mammals are attracted towards some of their natural predators, often without overt aggression. The biological function of this predator attraction was studied in a colony of herring gulls and lesser black-backed gulls, with the aid of predator models. More birds flocked above the predator model when it was presented together with a dead gull; also the birds did not land as close to a predator with a dead gull as they did to a predator alone. Having seen a predator with a dead gull had a clear effect on the distance at which birds later avoided that particular predator on the ground when it was presented to them alone. It is suggested that predator-attraction enables animals to collect information about a potential enemy; in this information the experience of conspecifics with the predator is taken into account; subsequent behaviour of the animals depends partly on this information. The increase in the avoidance distance with respect to a predator with a dead bird may be an adaptation to carnivores' habit of surplus killing.     

A Test of the Multi-Predator Hypothesis: Rapid Loss of Antipredator Behavior after 130 years of Isolation

Many species find themselves isolated from the predators with which they evolved. Isolation often leads to the loss of costly antipredator behavior, which may have adverse consequences if the population should later come into contact with predators. An understanding of both the mechanism (i.e. the degree to which antipredator behavior depends on experience), and of the time course of loss is important to be able to predict how a population will respond to future contact. We studied ‘group‐size effects’– the way in which animals change the time they allocate to antipredator vigilance as a function of group size – and visual and acoustic predator recognition in a population of tammar wallabies (Macropus eugenii), a cat‐sized (6–10 kg) macropodid marsupial. To study group size effects we observed wallabies foraging in four populations – three with some sort of predator and a New Zealand population that was isolated from all predators for about 130 yr. To study predator recognition, we observed the response of New Zealand wallabies to the presentation of a model or taxidermic mount of mammalian predators, and to the broadcast sounds of mammalian and avian predators. We compare these predator recognition experiments with results from a previous study of Kangaroo Island (South Australia) tammars. Complete isolation from all predators for as few as 130 yr led to the loss of group size effects and a rapid breakdown in visual predator recognition abilities. Our results are consistent with a key prediction of the multi‐predator hypothesis – namely, that the isolation from all predators may lead to a rapid loss of antipredator behavior.     

8. CORRESPONDENCE

This paper investigates, through experiments using surrogate predators, differences in intraspecific alarm calls between familiar and unfamiliar Bronze Mannikin Spermestes cucculatus groups. Four groups of mannikins were captured with mist nets from four areas in Durban (i.e. original groups) and randomly mixed (i.e. assorted groups). These groups were exposed to latex terrestrial snakes and mounted aerial raptors, and their alarm calls and predator response behaviours recorded. The Bronze Mannikins were able to discriminate between predators of different sizes, and increased their calling rate and decreased the end frequency of the alarm call in response to larger predators. This perhaps signalled increased threat, while simultaneously decreasing the conspicuousness of the flock. When the alarm call structure of the original and assorted groups in response to both raptors and snakes was compared, birds in original groups called more often, but paused longer between calls. Anti-predator behaviour differed in that assorted groups were less vigilant and aggressive toward the predators and panicked more frequently. In these groups, a failure to transfer the predation threat information might have caused the group to stop behaving cohesively and reliably. The manipulated experiments carried out in this study indicated that Bronze Mannikins were able to communicate predator size risk to conspecifics, but not as successfully to unfamiliar group members, showing that the investment, probability through altruistic payback, is greater in stable groups.     

Predator‐Naïve Brown Trout (Salmo trutta) Show Antipredator Behaviours to Scent from an Introduced Piscivorous Mammalian Predator Fed Conspecifics

Introduced mammalian predators may pose a high risk for native and naïve prey populations, but little is known about how native fish species may recognize and respond to scents from introduced mammalian predators. We investigated the role of diet‐released chemical cues in facilitating predator recognition, hypothesizing that native brown trout (Salmo trutta) would exhibit antipredator behaviours to faeces scents from the introduced American mink (Neovision vison) fed conspecifics, but not to non‐trout diets. In treatments‐control and replicate stream tank experiments, brown trout showed significant antipredator responses to faeces scent from mink fed conspecifics, but not to faeces scent from mink fed a non‐trout diet (chicken), or the non‐predator food control, Eurasian beaver (Castor fiber). We conclude that native and naïve brown trout show relevant antipredator behaviours to an introduced mammalian predator, presumably based on diet‐released conspecific alarm cues and thereby estimate the predation risk.     

Recognition and Response to Native and Novel Predators in the Largespring mosquitofish,Gambusia geiseri

The introduction of predator species into new habitats is an increasingly common consequence of human activities, and the persistence of native prey species depends upon their response to these novel predators. In this study, we examined whether the Largespring mosquitofish, Gambusia geiseri exhibited antipredator behavior and/or an elevation of circulating stress hormones (cortisol) to visual and chemical cues from a native predator, a novel predator, or a non‐predatory control fish. Prey showed the most pronounced antipredator response to the native predator treatment, by moving away from the stimulus, while the prey showed no significant changes in their vertical or horizontal position in response to the novel or non‐predator treatments. We also found no significant difference in water‐borne cortisol release rates following any of the treatments. Our results suggest the prey did not recognize and exhibit antipredator behavior to the novel predator, and we infer that this predator species could be detrimental if it expands into the range of this prey species. Further, our study demonstrates prey may not respond to an invasive predator that is phylogenetically, behaviorally, and morphologically dissimilar from the prey species' native predators.     

Kea Nestor notabilis mothers produce nest-specific calls with low amplitude and high entropy

Vocal behaviour of nesting altricial birds is subject to selection pressure from several sources. Offspring beg to attract parents’ attention, thus increasing the chances of being fed, but also increasing the chances of being detected by predators. Research on passerines has shown that parents may reduce the risk of nest predation by alarm calling to warn nestlings to be quiet, and by producing food calls which solicit begging when parents are present to defend the nestlings. Both nestlings and parents may reduce the risk of predator detection by producing calls of low amplitude and high entropy which are acoustically difficult to locate. Although extensive research has been undertaken on nesting passerine vocalizations, little is known about parrots in this regard, and studies are needed to determine whether parrots show similar adaptations. We investigated the calling behaviour of Kea Nestor notabilis mothers during the nesting period to determine whether maternal vocalizations were adapted in a way that could increase the chance of brood success. A microphone was installed inside the nest to record calls produced both inside the nest and in the direct vicinity. Our prediction was that calls outside the nest would be easy to locate and could function as alarm calls to alert conspecifics or distract the predator, whereas calls inside the nest would be difficult to locate and could serve to communicate with nestlings without alerting predators. Our results accorded with these predictions. Calls produced outside the nest were loud and tonal, and corresponded to previously described Kea alarm calls. Calls produced inside the nest, however, were high-entropy and low-amplitude calls, and formed a distinct structural category. We thus provide the first evidence that a parrot species has a vocal category for communication inside the nest, and that calls within this category are structured in a way that could reduce the risk of nest predation.     

Behavioural response evoked by conspecific distress calls in two neotropical treefrogs

Anurans emit distress calls when attacked by predators as a defensive mechanism. As distress calls may trigger antipredator behaviour even in individuals that are not under attack, we tested whether this defensive behaviour induced behavioural changes in neighbouring conspecifics. We compared the behavioural responses of two species of Neotropical hylid frogs (genus Boana) to conspecific distress calls and white noise. Individuals of both species interrupted their vocal activity and decreased call rate after hearing the distress call. Natural variation on signal intensity calibrated among the nearest neighbours did not influence the response and we did not observe negative phonotaxis after any acoustic stimulus. Despite the fact that many predators are acoustically oriented, we could not determine if such response (reduced call rate) was induced by risk assessment or by the masking effect on advertisement calls. Boana faber responded similarly to white noise and distress calls, while B. bischoffi responded more intensely to distress calls. Duration of silence after playbacks in B. faber was longer than B. bischoffi. We suggest that, if the signals are interpreted as a risk cue by neighbouring conspecifics, each species may be preyed upon by different predators, as they may have led to distinct defensive strategies and different responses to distress calls. If risk assessment information is included in distress calls, it triggers behavioural responses only in the nearest neighbours, as we did not observe responses on the vocal activity of the interspecific chorus. Our results add relevant data about acoustic communication and interpretations by anurans, highlighting the importance of considering cues within common and widespread signals.     

Distress Calls of Birds in a Neotropical Cloud Forest1

Distress calls are loud, harsh calls given by some species of birds when they are captured by a predator or handled by humans. We recorded the frequency of distress calls and struggling behavior in 40 species of birds captured in mist nets during the dry season in a Costa Rica cloud forest. We tested the following hypotheses proposed to explain the function of distress calls: (1) calling for help from kin or reciprocal altruists; (2) warning kin; (3) eliciting mobbing behavior; (4) startling the predator; and (5) distracting the predator through attraction of additional predators. Our results did not support the calling‐for‐help, warning kin, or mobbing hypotheses. Indeed, genera that regularly occurred with kin or in flocks were not more likely to call than non‐flocking genera. There was no relationship between calling frequency and struggling behavior as predicted by the predator startle hypothesis. Genera of larger birds tended to call more than smaller birds, providing some support for both the predator distraction hypothesis and predator startle hypotheses. Calls of higher amplitude may be more effective in startling the predator. Distress calls of larger birds may also travel greater distances than those of smaller birds, supporting the predator manipulation hypothesis, but this requires further testing.     

Effects of predator-specific defence on biodiversity and community complexity in two-trophic-level communities

Summary Antipredator strategies employed by prey may be specific (effective against only one type of predator) or non-specific (effective against all predators). To examine the effects of the specificity of antipredator behaviour on biodiversity and community complexity, we analyse mathematical models including both evolutionary and population dynamics of a system including multiple prey species and multiple predator species. The models assume that all predator species change in their prey choice and all prey species have evolutionary change in their antipredator effort in evolution. The traits of each species change in an adaptive manner, whose rate is proportional to the slope of their fitness function. We calculate community complexity, resource-overlap between predators, an index of biodiversity and other properties of the coevolutionarily stable community for two cases: (1) all prey species have non-specific antipredator behaviour and (2) all prey species have predator-specific defence. Predator-specificity in defence increases community complexity, resource-overlap between predators, the total abundance of predators and the ratio of predator to prey abundance. Specific defence also decreases the number of isolated subwebs within the entire foodweb.