A host-race of the cuckoo Cuculus canorus with nestlings attuned to the parental alarm calls of the host species

The common cuckoo has several host-specific races, each with a distinctive egg that tends to match its host's eggs. Here, we show that the host-race specializing on reed warblers also has a host-specific nestling adaptation. In playback experiments, the nestling cuckoos responded specifically to the reed warbler's distinctive 'churr' alarm (given when a predator is near the nest), by reducing begging calls (likely to betray their location) and by displaying their orange-red gape (a preparation for defence). When reed warbler-cuckoos were cross-fostered and raised by two other regular cuckoo hosts (robins or dunnocks), they did not respond to the different alarms of these new foster-parents. Instead, they retained a specific response to reed warbler alarms but, remarkably, increased both calling and gaping. This suggests innate pre-tuning to reed warbler alarms, but with exposure necessary for development of the normal silent gaping response. By contrast, cuckoo chicks of another host-race specializing on redstarts showed no response to either redstart or reed warbler alarms. If host-races are restricted to female cuckoo lineages, then chick-tuning in reed warbler-cuckoos must be under maternal control. Alternatively, some host-races might be cryptic species, not revealed by the neutral genetic markers studied so far.     

A mutual understanding? Interspecific responses by birds to each other's aerial alarm calls

Individuals are likely to benefit from responding to the alarmsignals of other species with similar predators, and mutualinterspecific responses to aerial (hawk) alarms are thoughtto be common in birds, in part because similarity in alarm callstructure among species might facilitate detection or interpretation.However, there has been no test of whether interspecific responsesto aerial alarm calls can involve mutual responses between speciesand only incomplete tests of the response of any species tosuch heterospecific alarms. We describe the aerial alarm callsof white-browed scrubwrens (Sericornis frontalis) and superbfairy-wrens (Malurus cyaneus) and use a playback experimentto test for mutual responses to each other's aerial alarm calls.The 2 species occur in similar habitats and can co-occur inmixed-species flocks during the nonbreeding season. The aerialalarm calls of both species are high pitched (7 kHz) and rapidlyfrequency-modulated calls but are distinct in frequency measuresand only the scrubwren's call had 2 parallel sounds. Both speciesfled to cover after playback of either their own or the otherspecies' alarm calls but never to control sounds. The responseto either species' alarm was almost invariant in both speciesin an experiment at high natural amplitude, but there was aslightly lower response to heterospecific compared with conspecificalarms when playbacks were at the mean natural amplitude. Ourresults demonstrate, after at least 50 years of interest inthe subject, that there can be mutual responses to aerial alarmcalls between species.     

Fork-tailed drongos use deceptive mimicked alarm calls to steal food

Despite the prevalence of vocal mimicry in animals, few functions for this behaviour have been shown. I propose a novel hypothesis that false mimicked alarm calls could be used deceptively to scare other species and steal their food. Studies have previously suggested that animals use their own species-specific alarm calls to steal food. However none have shown conclusively that these false alarms are deceptive, or that mimicked alarm calls are used in this manner. Here, I show that wild fork-tailed drongos (Dicrurus adsimilis) make both drongo-specific and mimicked false alarm calls when watching target species handling food, in response to which targets flee to cover abandoning their food. The drongo-specific and mimicked calls made in false alarms were structurally indistinguishable from calls made during true alarms at predators by drongos and other species. Furthermore, I demonstrate by playback experiments that two of these species, meerkats (Suricata suricatta) and pied babblers (Turdoides bicolor), are deceived by both drongo-specific and mimicked false alarm calls. These results provide the first conclusive evidence that false alarm calls are deceptive and demonstrate a novel function for vocal mimicry. This work also provides valuable insight into the benefits of deploying variable mimetic signals in deceptive communication.     

Context-dependent vocal mimicry in a passerine bird

How do birds select the sounds they mimic, and in what contexts do they use vocal mimicry? Some birds show a preference for mimicking other species' alarm notes, especially in situations when they appear to be alarmed. Yet no study has demonstrated that birds change the call types they mimic with changing contexts. We found that greater racket-tailed drongos (Dicrurus paradiseus) in the rainforest of Sri Lanka mimic the calls of predators and the alarm-associated calls of other species more often than would be expected from the frequency of these sounds in the acoustic environment. Drongos include this alarm-associated mimicry in their own alarm vocalizations, while incorporating other species' songs and contact calls in their own songs. Drongos show an additional level of context specificity by mimicking other species' ground predator-specific call types when mobbing. We suggest that drongos learn other species' calls and their contexts while interacting with these species in mixed flocks. The drongos' behaviour demonstrates that alarm-associated calls can have learned components, and that birds can learn the appropriate usage of calls that encode different types of information.     

Parental Alarm Calls of the White‐Crowned Sparrow Fail to Stimulate Corticosterone Production in Nest‐Bound Offspring

Alarm calling by parents is widespread among animals and has strong implications for parent and offspring fitness, yet it is virtually unknown whether parental alarm calls can initiate a corticosterone response in offspring. We investigated whether parental alarm calls of the white‐crowned sparrow, Zonotrichia leucophrys, activated the corticosterone response of their nest‐bound young, as such a response might prepare older nestlings for premature fledging and increase their survival when contacted by a predator at the nest. We conducted an experiment in which nestlings were either exposed to parent alarm calls (treatment) or experienced a period without parental alarm calls (control) immediately prior to blood sampling. We then sampled nestlings to measure corticosterone levels within 4 min of first contact (baseline corticosterone) and 60 min later (handling‐induced corticosterone). Young nestlings (i.e. 3–4 d post‐hatch) did not exhibit a corticosterone response to parental alarm calls or to handling, as mean corticosterone levels were similar in the control and treatment groups for both baseline and 60‐min post‐baseline samples. Against our predictions, there was no difference in mean levels of baseline corticosterone between control and treatment groups in older nestlings (i.e. 7?8 d post‐hatch) that were capable of surviving out of the nest. However, we did find a significant increase in mean levels of corticosterone after handling in both groups, which indicated that older nestlings were able to mount a functional corticosterone response when confronted with a potential predator. Why older nestlings did not initiate a corticosterone response after exposure to parental alarm calls is unclear but may have occurred because the costs of mounting such a response outweighed the benefits, perhaps because of growth or developmental costs.     

Does Gray Squirrel (Sciurus carolinensis) Response to Heterospecific Alarm Calls Depend on Familiarity or Acoustic Similarity?

In habitats in which multiple species are prey to the same predators, individuals can greatly benefit from recognizing information regarding predators that is provided by other species. Past studies have demonstrated that various mammals respond to familiar heterospecific alarm calls, but whether acoustic similarity to a familiar call can prompt a mammal's recognition of an unfamiliar call has yet to be shown. We presented alarm calls to free‐ranging eastern gray squirrels (Sciurus carolinensis) and recorded behavioral changes in vigilance and antipredatory response. Playbacks included alarm calls of a sympatric bird (American robin, Turdus migratorius), an allopatric bird with a call structure similar to that of the robin (common blackbird, Turdus merula), and an allopatric bird with a distinct call structure (New Holland honeyeater, Phylidonyris novaehollandiae). Squirrels responded significantly more frequently to squirrel alarm calls (positive control) than to robin song (negative control) or honeyeater calls. Squirrel response to robin and blackbird alarm calls was statistically similar to their response to squirrel alarm calls, indicating that squirrels responded to those alarm calls as if they provided information about the presence of predators. However, squirrel response to robin song was not statistically different from response to any of the other avian calls, including the robin and blackbird alarms, suggesting that squirrels neither respond to blackbird alarms as if they clearly signify danger, nor as if they clearly do not signify danger, perhaps reflecting some ambiguity in interpretation of the calls. These results suggest that squirrel responses to alarm calls are generally based on call familiarity, but that acoustic similarity of an unfamiliar allopatric call to a familiar call also can elicit antipredator behavior. The lack of response to honeyeater alarm calls also supports the hypothesis that call recognition by gray squirrels is dependent on familiarity, rather than simply detection of an acoustic feature common to alarm calls across a variety of avian species.     

Adaptive differences in response to two types of parental alarm call in altricial nestlings

Vertebrate alarm calls can contain information about the type of predator and the degree of danger, but young animals often respond to alarm calls differently from adults. The distinct behaviour of young may reflect an imperfect stage in the gradual development of the adult response, or a response adapted to specific risks faced by young. In this study, we tested whether nestling white-browed scrubwrens, Sericornis frontalis, responded to different alarm calls according to their specific risks of predation. As predators on the ground pose a danger to scrubwren nestlings, whereas flying predators do not, we predicted that they would respond to ground alarm calls but not to aerial alarm calls. In a field playback experiment, we tested the response of young to aerial and ground alarm calls, each presented in a shorter (less urgent) and longer (more urgent) form. We found that both 5- and 11-day-old nestlings responded to ground alarm calls, and did so more strongly to the more urgent playback. By contrast, the response to aerial alarm calls started to develop only towards the end of the nestling stage. Thus, scrubwren nestlings can distinguish between different types of alarm calls and react more strongly to calls warning of a predator posing greater danger, appropriate to the nestling stage of development. Furthermore, they use the length of ground alarm calls as an indicator of the degree of danger.     

A host-race difference in begging calls of nestling cuckoos Cuculus canorus develops through experience and increases host provisioning

The structure of common cuckoo nestling begging calls differs between the two host-races parasitizing reed warblers (reed warbler-cuckoos) and dunnocks (dunnock-cuckoos; longer syllable duration, lower peak and maximum frequency, narrower bandwidth). Cross-fostering experiments demonstrated that this difference is not genetically fixed but develops through experience. When newly hatched reed warbler-cuckoos were transferred to dunnock nests, they developed begging calls more like those of dunnock-cuckoos, whereas controls transferred to the nests of robins or left to be raised by reed warblers developed calls more typical of reed warbler-cuckoos. We tested the effectiveness of these different calls in stimulating host provisioning by placing in host nests a single blackbird or song thrush nestling (of similar size to a young cuckoo, but lacking its exuberant begging calls); when it begged we broadcast, from a small loudspeaker on the nest rim, recordings of either dunnock-cuckoo or reed warbler-cuckoo begging calls. Playback of dunnock-cuckoo begging calls induced higher levels of provisioning by dunnocks, whereas playback of reed warbler-cuckoo begging calls did so for both reed warblers and robins. We suggest that the young cuckoo (which ejects the host's eggs/chicks and so is raised alone) learns by experience which calls best stimulate host provisioning.     

Crying wolf to a predator: deceptive vocal mimicry by a bird protecting young

Animals often mimic dangerous or toxic species to deter predators; however, mimicry of such species may not always be possible and mimicry of benign species seems unlikely to confer anti-predator benefits. We reveal a system in which a bird mimics the alarm calls of harmless species to fool a predator 40 times its size and protect its offspring against attack. Our experiments revealed that brown thornbills (Acanthiza pusilla) mimic a chorus of other species'' aerial alarm calls, a cue of an Accipiter hawk in flight, when predators attack their nest. The absence of any flying predators in this context implies that these alarms convey deceptive information about the type of danger present. Experiments on the primary nest predators of thornbills, pied currawongs (Strepera graculina), revealed that the predators treat these alarms as if they themselves are threatened by flying hawks, either by scanning the sky for danger or fleeing, confirming a deceptive function. In turn, these distractions delay attack and provide thornbill nestlings with an opportunity to escape. This sophisticated defence strategy exploits the complex web of interactions among multiple species across several trophic levels, and in particular exploits a predator''s ability to eavesdrop on and respond appropriately to heterospecific alarm calls. Our findings demonstrate that prey can fool predators by deceptively mimicking alarm calls of harmless species, suggesting that defensive mimicry could be more widespread because of indirect effects on predators within a web of eavesdropping.     

Effect of conspecific alarm calls in the parental behaviour of nesting southern house wrens

Alarm calls are usually used to signal the presence of a threat to members of the same species and have been studied broadly in social foraging species. We analysed the effects of conspecific alarm calls on the parental behaviour of a territorial species, the southern house wrens (Troglodytes aedon musculus), during nestling stage. We compared the parental response of adults feeding 9–11-day-old nestlings when faced with conspecific alarm calls and with a control non-sympatric species’ song broadcast from a neighbouring territory. We measured the time required by parents to return to the nest (latency) when exposed to the stimuli and estimated parent’s nest visitation rate and mean visit duration. Parents took longer to resume parental activities when we broadcast a conspecific alarm call, but they did not modify their nest visitation rate or the mean visit duration. Heterospecific songs did not seem to affect parental behaviour. Our results suggest that nesting southern house wrens can use alarm calls uttered from neighbouring territories to assess the presence of a threat and adjust their parental behaviour accordingly.     

Decrease in Alarm Call Response Among Tufted Capuchins in Competitive Feeding Contexts: Possible Evidence for Counterdeception

Animal signals function to elicit behaviors in receivers that ultimately benefit the signaler, while receivers should respond in a way that maximizes their own fitness. However, the best response may be difficult for receivers to determine when unreliable signaling is common. “Deceptive” alarm calling is common among tufted capuchins (Cebus apella nigritus) in competitive feeding contexts, and responding to these calls is costly. Receivers should thus vary their responses based on whether a call is likely to be reliable. If capuchins are indeed able to assess reliability, I predicted that receivers will be less likely to respond to alarms that are given during competitive feeding contexts than in noncompetitive contexts, and, within feeding contexts, that individuals inside or adjacent to a food patch will be less likely to respond to alarms than those further from the resource. I tested these predictions in a group of wild capuchins by observing the reactions of focal animals to alarm calls in both noncompetitive contexts and experimental feeding contexts. Antipredator escape reactions, but not vigilance reactions, occurred significantly less often in competitive feeding contexts than in noncompetitive contexts and individuals adjacent to food patches were more likely to respond to alarm calls than were those inside or further from food patches. Although not all predictions were fully supported, the findings demonstrate that receivers vary their behavior in a way that minimizes the costs associated with “deceptive” alarms, but further research is needed to determine whether or not this can be attributed to counterdeception.     

Development of stress response in nestling pied flycatchers

Birds respond to unpredictable events by secreting corticosterone, which induces various responses to cope with stressful situations. However, the evidence is still elusive whether altricial nestlings perceive and respond to external stressors. We investigated the development of adrenocortical stress response to handling-related stressor in nestlings of a small passerine bird, the pied flycatcher (Ficedula hypoleuca). Nestlings were held in isolation from their parents during the experiment to ensure that they indeed respond to handling, not to parental alarm calls. We found that both 9- and 13-day-old nestlings were able to elicit hormonal stress response. Although baseline as well as stress-induced corticosterone levels rose slightly with age, the magnitude of difference between the control and stress-induced levels remained similar in both age groups. However, comparison with adults showed that the stress response of nestlings prior to fledging was still incomplete and significantly lower than in adults. Overall, our results indicate that altricial nestlings do respond to acute stressors, but on the contrary to previous predictions the development of corticosterone stress response during growth period is not gradual and varies remarkably between different passerine species.     

Parental alarm calls suppress nestling vocalization

Evolutionary models suggest that the cost of a signal can ensure its honesty. Empirical studies of nestling begging imply that predator attraction can impose such a cost. However, parents might reduce or abolish this cost by warning young of the presence of danger. We tested, in a controlled field playback experiment, whether alarm calls cause 5-, 8- and 11-day-old nestlings of the white-browed scrubwren, Sericornis frontalis, to suppress vocalization. In this species, nestlings vocalize when parents visit the nest ('begging') and when they are absent ('non-begging'), so we measured effects on both types of vocalization. Playback of parental alarm calls suppressed non-begging vocalization almost completely but only slightly reduced begging calls during a playback of parental feeding calls that followed. The reaction of nestlings was largely independent of age. Our results suggest two reasons why experiments ignoring the role of parents probably overestimate the real cost of nestling vocalizations. Parents can warn young from a distance about the presence of danger and so suppress non-begging vocalizations that might otherwise be overheard, and a parent's presence at the nest presumably indicates when it is safe to beg.     

Functionally Referential Alarm Calls in Tamarins (Saguinus fuscicollis and Saguinus mystax) – Evidence from Playback Experiments

Studies on primate vocalisation have revealed different types of alarm call systems ranging from graded signals based on response urgency to functionally referential alarm calls that elicit predator‐specific reactions. In addition, alarm call systems that include both highly specific and other more unspecific calls have been reported. There has been consistent discussion on the possible factors leading to the evolution of different alarm call systems, among which is the need of qualitatively different escape strategies. We studied the alarm calls of free‐ranging saddleback and moustached tamarins (Saguinus fuscicollis and Saguinus mystax) in northeast Peru. Both species have predator‐specific alarm calls and show specific non‐vocal reactions. In response to aerial predators, they look upwards and quickly move downwards, while in response to terrestrial predators, they look downwards and sometimes approach the predator. We conducted playback experiments to test if the predator‐specific reactions could be elicited in the absence of the predator by the tamarins’ alarm calls alone. We found that in response to aerial alarm call playbacks the subjects looked significantly longer upwards, and in response to terrestrial alarm call playbacks they looked significantly longer downwards. Thus, the tamarins reacted as if external referents, i.e. information about the predator type or the appropriate reaction, were encoded in the acoustic features of the calls. In addition, we found no differences in the responses of S. fuscicollis and S. mystax whether the alarm call stimulus was produced by a conspecific or a heterospecific caller. Furthermore, it seems that S. fuscicollis terrestrial alarm calls were less specific than either S. mystax terrestrial predator alarms or either species’ aerial predator alarms, but because of the small sample size it is difficult to draw a final conclusion.     

Begging to differ: scrubwren nestlings beg to alarm calls and vocalize when parents are absent

Nestling birds face a dilemma: they can increase parental provisioning by begging more intensively, but by doing so may also increase their risk of predation. Nestlings could deal with this dilemma by reducing begging intensity after parents have warned them of a nearby predator. We therefore tested experimentally whether nestling scrubwrens, Sericornis frontalis, increase begging intensity with hunger but reduce it after adult alarm calls. Single 5- and 8-day-old nestlings were temporarily taken into the laboratory for playback experiments. Over a 90-min period of food deprivation we simulated parental visits every 10 min by playing back adult feeding calls. Hungrier nestlings begged louder and longer to simulated parental visits, but contrary to expectation did not beg less if they had previously heard playback of alarm calls, and even begged to the alarm calls themselves. The results were similar for both ‘mobbing’ and ‘flee’ alarm calls. Nestlings also gave distinctive calls in the 10-min interval between simulated parental visits, and the number of these calls increased with hunger and after playback of alarm calls. We suggest that nestlings acquire the ability to respond appropriately to alarm calls late in the nestling period and that therefore parents might be selected to avoid alarm calling when defending young nestlings.Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Alarm calls of wintering great tits Parus major: warning of mate,reciprocal altruism or a message to the predator?

When a predator is not an immediate threat, a prey may produce relatively loud alarm calls because the risk is low. Since such calls could nevertheless attract acoustically oriented predators, the cost of predator attraction must be outweighed by factors beneficial to the caller. In this field study we elicited low-risk alarm calls by temporarily catching wintering adult male great tits Parus major at feeders both within and outside their territories. We tested whether the alarm calls of dominant males can be explained in terms of mate warning, reciprocal altruism or notifying the predator of detection. If alarms are intended to warn mates, males accompanied by their mates should give alarm calls both within and outside home range, even if other permanent flock members are absent. If alarms are to be explained by reciprocal altruism, male great tits should give low-risk alarm calls when accompanied by permanent flock members other than mate within and not outside of the home-range. If alarm calling is a message to a predator, males should call when foraging alone. We found that male great tits gave low-risk alarm calls when accompanied by their mates, independent of feeder location. They also gave low-risk alarm calls within home ranges in the presence of other permanent flock members when mates were absent. In contrast, only a few males gave calls when foraging alone within their home ranges, or when in the company of unfamiliar great tits outside their usual home-range. The results suggest that the utterance of alarm calls may be explained as mate protection and reciprocal altruism among familiar individuals.     

Effect of alarm calling by male Red‐winged Blackbirds on nestling begging and female provisioning behavior

ABSTRACT Nestling begging and parental provisioning can attract nest predators and reduce reproductive success, so parents and their offspring might be expected to respond adaptively by minimizing predator‐attracting cues when predators threaten nests. Male Red‐winged Blackbirds (Agelaius phoeniceus) are well known for their antipredator alarm calls that contain information about the approach of potential nest predators. We examined the begging behavior of nestlings and the provisioning behavior of females in response to antipredator alarm calls of males to test the adaptive response hypothesis. Playback experiments provided no evidence that alarm calls function to switch off vocal begging; nestlings were equally likely to beg vocally during playback and control periods. Video recordings showed that male alarm calling had no significant effect on inappropriate vocal begging (in the absence of an adult), but significantly reduced the incidence of spontaneous calling (in the absence of begging). Adult females responded to male antipredator alarm calls by delaying their provisioning visits. In addition, although having no significant effect on use of nest‐arriving calls by females, male alarm calling significantly reduced their use of nest‐leaving calls. We conclude that nestling and female Red‐winged Blackbirds respond to male alarm calls in ways that might reduce the risk of predation, but nestlings beg vocally when females arrive to feed them, regardless of male alarm calling, perhaps to avoid a competitive disadvantage with broodmates.     

Ambient noise increases missed detections in nestling birds

Ambient noise can mask acoustic cues, making their detection and discrimination difficult for receivers. This can result in two types of error: missed detections, when receivers fail to respond to the appropriate cues, and false alarms, when they respond to inappropriate cues. Nestling birds are error-prone, sometimes failing to beg when parents arrive with food (committing missed detections) or begging in response to stimuli other than a parent's arrival (committing false alarms). Here, we ask whether the frequency of these errors by nestling tree swallows (Tachycineta bicolor) increases in the presence of noise. We found that nestlings exposed to noise had more missed detections than their unexposed counterparts. We also found that false alarms remained low overall and did not differ significantly between noise and quiet treatments. Our results suggest that nestlings living in noisy environments may be less responsive to their parents than nestlings in quieter environments.     

Human adoption in evolutionary perspective

Exploitation is a fundamental element of the parental strategies of many species of birds. Cuckoos, for example, lay their eggs in the nest of other birds, who often unwittingly rear the alien nestlings as their own. Nest parasitism is an efficient reproductive strategy for cuckoos, who do not have to worry about building a nest, incubating their eggs, or feeding their nestlings. But not all hosts respond passively to such intrusions. In response to parasitic cowbirds, for example, robins have evolved the ability to detect and selectively eject alien young from their nests. Human parenting strategies differ sharply from the strategies of cuckoos and robins. Unlike cuckoos, we are reluctant to allow our children to be raised by others. Unlike robins, we knowingly rear strange young. What makes human behavior toward children so different from that of cuckoos and robins? Humans seem to share a number of predispositions that facilitate successful adoptive relationships, and the desire to raise children seems to be pervasive among modern humans. Despite these commonalities, patterns of adoption transactions vary greatly among contemporary human societies. This paper considers the origins and causes of cross-cultural variation in human adoptive behavior from an evolutionary perspective.     

Observed instances of alarm calling in the Cape Rockjumper

Here I give an account of alarm calls recorded during behavioural observations on Cape Rockjumpers (CRJs) and the potential predators observed nearby. I found CRJs did not produce alarm calls in the presence of Boomslang (a previously known predator of CRJ nestlings), whereas they did produce alarm calls in the presence of Rock Kestrels, which was unexpected as previous literature suggested Rock Kestrels do not prey upon CRJ. However, during field observations I witnessed a Rock Kestrel attack an adult CRJ, suggesting that Rock Kestrels may opportunistically prey upon CRJs. Further studies on site- and temporal-specificity in CRJs may lead to additional understanding of the flexibility of alarm calling in group-living species.