Cuckoo–hawk mimicry? An experimental test

The similarity between many Old World parasitic cuckoos (Cuculinae) and Accipiter hawks, in size, shape and plumage, has been noted since ancient times. In particular, hawk-like underpart barring is more prevalent in parasitic than in non-parasitic cuckoos. Cuckoo-hawk resemblance may reflect convergent evolution of cryptic plumage that reduces detection by hosts and prey, or evolved mimicry of hawks by parasitic cuckoos, either for protection against hawk attacks or to facilitate brood parasitism by influencing host behaviour. Here, we provide the first evidence that some small birds respond to common cuckoos Cuculus canorus as if they were sparrowhawks Accipiter nisus. Great tits and blue tits were equally alarmed and reduced attendance at feeders during and after the presentation of mounted specimens of common cuckoos and sparrowhawks, but not in response to control presentations of collared doves or teal. Plumage manipulations revealed that the strong alarm response to cuckoos depended on their resemblance to hawks; cuckoos with barred underparts were treated like hawks, while those with unbarred underparts were treated like doves. However, barring was not the only feature inducing alarm because tits showed similarly strong alarm to barred and unbarred hawks, and little alarm to barred doves. These responses of tits, unsuitable as hosts and hence with no history of cuckoo parasitism, suggest that naive small birds can mistake cuckoos for hawks. Thus, any cuckoo-hawk discrimination by host species is likely to be an evolved response to brood parasitism.     

Hawk mimicry in cuckoos and anti‐parasitic aggressive behavior of barn swallows in Denmark and China

Hosts of brood parasites defend their nests against parasitism by aggression and subsequently, if parasitized, by rejection of the parasite egg or nestling. Cuckoos have evolved plumage mimicry with convergence towards the phenotype of Accipiter hawks that are common predators of cuckoo hosts. Here we tested two alternative hypotheses 1) whether barn swallows Hirundo rustica have evolved less aggressive behavior towards cuckoos in areas of sympatry with more abundant Accipiter hawks; and 2) whether barn swallows have evolved more aggressive anti‐parasite behavior in areas with a single species of cuckoo. We presented dummies of common cuckoo Cuculus canorus, sparrowhawk Accipiter nisus and Oriental turtledove Streptopelia orientalis (a benign control) at the nests of barn swallows during breeding, while recording intensity of response and proximity of barn swallows to the dummy. We demonstrated that cuckoos moved away when attacked aggressively and approached more closely by barn swallows showing that barn swallow behavior was efficient at driving away cuckoos. Barn swallows were significantly more aggressive and approached cuckoo and sparrowhawk dummies more closely in Denmark than in China, despite sparrowhawks being relatively more common in Denmark. Responses towards cuckoo dummies differed from responses towards sparrowhawk dummies, showing that barn swallows distinguished between the two different causes of danger. These findings are inconsistent with a less aggressive response towards cuckoo dummies in areas of sympatry with more abundant Accipiter hawks, but consistent with the alternative hypothesis that barn swallows have evolved more aggressive behavior towards cuckoos in areas with a single species of brood parasite, but not in areas with multiple species of parasites, where it is harder for hosts to tell the difference.     

The function of three main call types in common cuckoo

Acoustic signals play a key role in shaping the relationships in birds. Common cuckoos Cuculus canorus are known to produce various call types, but the function of these calls has only been studied recently. Here, we used a combination of field recordings (conducted in 2017) and playback experiments (conducted in 2018) to investigate the functional significance of common cuckoo calls. We found significant differences in the characteristics between male two‐element “cu‐coo” and three‐element “cu‐cu‐coo” calls, with these two call types being used in different contexts. The three‐element male “cu‐cu‐coo” calls were associated with females emitting their “bubbling” call. Playback experiments revealed that both males and females exhibit stronger responses to playing female “bubbling” calls than with the calls of the Eurasian sparrowhawk (Accipter nisus) serving as a control, suggesting a significant intraspecific communication function for this call type. However, we did not find any evidence to support mate attraction in male calls, as females were not stimulated by playback of male calls compared with sparrowhawk calls in the control group.     

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.     

Great tits take greater risk toward humans and sparrowhawks in urban habitats than in forests

Urban animals often take more risk toward humans than their non‐urban conspecifics do, but it is unclear how urbanization affects behavior toward non‐human predators. Responses to humans and non‐human predators may covary due to common mechanisms enforcing a phenotypic correlation. However, while increased tolerance toward humans may be advantageous for urban animals, reduced vigilance toward non‐human predators that can pose actual threat may be costly. Therefore, urban animals may benefit from showing specific responses to different threat levels, such as humans versus non‐human predators, or hostile versus non‐hostile humans. To test these alternatives, we compared responses (latencies to return to nest) of urban and forest‐breeding great tits (Parus major) to familiar hostile and unfamiliar humans as well as one of their common predators, the sparrowhawk (Accipiter nisus). We found that urban birds were more risk‐taking toward both humans and sparrowhawk than forest birds. However, responses to sparrowhawk did not correlate with responses to humans either within or across habitats. This suggests that higher risk‐taking of urban compared to forest‐dwelling great tits toward sparrowhawk may be threat‐specific response to lower predation risk rather than a spillover effect of increased tolerance to humans. Furthermore, birds responded similarly to unfamiliar and familiar (potentially dangerous) humans in both habitats, suggesting that great tits may not adjust their risk‐taking to the threat represented by individual humans. These findings indicate that urban birds may flexibly adjust their risk‐taking to certain, but not all, types of threat.     

Syntax manipulation changes perception of mobbing call sequences across passerine species

Many species approach predators to harass them and drive them away. Both the intensity of this antipredator strategy and its success are positively related to the size of the group that carries out this mobbing. To recruit individuals to the mob, members of prey species produce mobbing calls. In some songbirds—the Japanese tit, Parus minor, and the southern pied babbler, Turdoides bicolor—mobbing calls are structurally complex and it has been suggested that they convey information by means of compositional syntax, when meaningful items are combined into larger units. These two species combine alert and recruitment calls into an alert and recruitment sequence when attracting conspecifics to cooperate in mobbing a predator. Whether this rudimentary, two‐call, compositional structure is used by other bird species in mobbing calls and how it can alter the ability of heterospecifics to adequately recognize mobbing calls is not well understood. Heterospecifics’ responses to mobs are critical to the success of the mobbing strategy, so it is of great importance to understand whether and how syntax influences these responses. To address these questions, we conducted two playback experiments. Firstly, we investigated whether the great tit, Parus major, extracts different meanings from different individual motifs (i.e., component calls), and from combined motifs in both natural and artificially reversed order. We found that great tits extract different meanings from the two motifs involved in mobbing calls and that they also discriminate for motif order reversal in the mobbing call sequence. Secondly, we investigated whether heterospecifics (the coal tit, Periparus ater, and the common chaffinch, Fringilla coelebs) are sensitive to syntax alteration of great tit mobbing calls. While chaffinches did not respond to great tit mobbing calls, coal tits were sensitive to mobbing call sequence reversal although they did not react in the same way as conspecific subjects. Overall, whereas our results indicate that tits are sensitive to call reversal, this is not to say that tits actually use compositional syntax to increase the information content.     

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.     

Interspecific aggression declines seasonally in breeding great tits Parus major

During the breeding season, great tits show aggression to protect their nest from intra‐ and interspecific intruders. Aggression is a labile trait that can be plastically expressed as a result of individual differences (e.g., personality), seasonal gradients in the costs and benefits of aggression, or other environmental components (e.g., number of competitors). Competitors may try to take over great tit nests, because the number of suitable nesting sites is limited, and great tits may guard high quality territories. Taking over a great tit nest may be especially fruitful in early phenological stages (egg laying) when great tits frequent their nests less often. However, great tits may compensate for this vulnerability by being more aggressive toward intruders during early nesting stages, a pattern that has already been established in an intraspecific context. Previous studies have shown that interspecific intruders were most likely to die from great tit aggression during great tit egg laying, suggesting great tits may also be more aggressive during this phase in an interspecific context. Here, I tested this hypothesis with simulated territorial intrusions in great tit territories using taxidermized blue tits Cyanistes caeruleus (hereafter called blue tit models). Great tit aggression (number of calls and approach distance toward blue tit model) was assayed during egg laying, incubation, and chick rearing in the breeding season of 2014. Although sample size was low due to a high fraction of non‐responders (n = 44 out of 89 assays across 26 out of 35 individuals), I found that great tits showed a seasonal decline in aggressiveness, which is congruent with intraspecific results on this study species. I discuss my findings in the context of differential adjustment to climate change between interspecific competitors.     

Ravens adjust their antipredatory responses to con‐ and hetero‐specific alarms to the perceived threat

Heterospecific alarm calls are typically found in situations where multiple species have a common predator. In birds, they are particularly common in mixed mixed‐species flocks. In species with highly developed social and cognitive abilities like corvids, there is the potential for differential responses to heterospecific vs. conspecific calls according to the riskiness of the habitat. We tested the responses of free‐ranging ravens (Corvus corax) to conspecific alarm calls and compared them to heterospecific alarm calls of jackdaws (Corvus monedula). We observed the proportion of ravens leaving the feeding site after the con‐ or hetero‐specific playback was presented in a situation of low threat (wild boar—Sus scrofa enclosure) and high threat of predation (wolf—Canis lupus enclosure). We show that ravens responded to conspecific calls more intensively at the wolves than at the wild boar, but the response to conspecific calls was in both enclosures stronger than to the control (great tit—Parus major song). The response to the heterospecific alarm was also stronger in the wolves’ enclosure, but it did not differ from control in the wild boar enclosure. These findings suggest that ravens are aware of the meaning of the jackdaw alarm calls, but they respond to it only in a situation of high predatory threat (wolves are present). In the wild boar enclosure, the ravens probably consider jackdaws warning against some other predator, very probably harmless to ravens. This interpretation requires further testing, as both enclosures differ also in respect to other parameters like food quality and shelter availability.     

Egg Rejection and Brain Size among Potential Hosts of the Common Cuckoo

Interspecific brood parasitism by the common cuckoo (Cuculus canorus) lowers host fitness, and has selected for discrimination and rejection of parasitic eggs in their commonly parasitized hosts. Cognitive demands needed to discriminate and reject cuckoo eggs may have led to augmentation of relative brain size among passerine hosts parasitized by cuckoos. This hypothesis predicts for across species positive relationships of brain size with rejection rate, host suitability and parasitism level. Here we test these predictions while controlling for phylogenetic, ecological and developmental factors known to affect brain size and egg rejection in a comparative study using the cuckoo and their hosts in Europe as a model system. Contrary to expected the rate of rejection of non‐mimetic cuckoo eggs covaried negatively with relative brain size across bird species. Either suitability as cuckoo host, which reflects long‐time duration of exposure to cuckoo parasitism, and level of parasitism, did not relate to brain size. Our results do not support the hypothesis that cuckoo parasitism was a main direct force affecting brain size variation across passerine hosts.     

Stabilizing selection on blue tit fledgling mass in the presence of sparrowhawks

Like British great tits, Belgian blue tits have a lower winter body mass when sparrowhawks are present. Since body mass affects manoeuvrability in small birds, tits may balance the risks of starvation and the risk of hawk predation by varying the amount of extra fat carried during winter. Predation pressure by sparrowhawks on young and inexperienced fledglings is at least as intense as that on the adults during winter. We therefore expected that tit fledgling body mass could also be reduced in the presence of sparrowhawks. In the years after one pair of sparrowhawks settled in a study plot, the mean body mass of blue tit fledglings was lower compared with that in years when there were no sparrowhawks. Furthermore, the shape of the curve relating juvenile survival to fledging mass changed, because the survival of the heaviest fledglings was reduced, which altered the selection differential of juvenile survival as a function of body mass from directional to stabilizing. Of seven published studies on the fledgling body mass–survival relation in tits, all three of the studies conducted in the absence of sparrowhawks showed the highest survival rates for the heaviest young, whereas in all four studies with sparrowhawks present this was no longer the case.     

Snake-like calls in breeding tits

Hole-nesting tits belonging to the family Paridae produce a hissing display that resembles the exhalatory hiss of a snake. When a predatory animal enters the nest hole of a tit, tits often hiss vigorously, while lunging their head forward and shaking their wings and tail, until the intruder retreats. We assessed the acoustic similarity between such hiss calls from 6 species of tits, snake hisses, and tit syllables used in alarm vocalizations, as well as white noise as a control. Tit hiss calls showed a high degree of similarity with snake hisses from 3 different snake families. Tit hisses had lower similarity to syllable alarm calls, suggesting convergence of tit hisses in their spectral structure. Hiss calls would only be effective in protecting nest boxes if nest predators responded to these calls. In order to test this hypothesis, we trained individual Swinhoe’s striped squirrels, Tamiops swinhoei hainanus, a common predator of egg and nestling tits, to feed at feeders in proximity to nest boxes. We compared the aversive response of squirrels to tit’s hiss calls and white noise, presented in random order. Squirrels showed a higher degree of avoidance of feeders when hiss calls were played back than when white noise was presented. In conclusion, our study suggests that hole-nesting birds have evolved convergent snake-like hiss calls, and that predators avoid to prey on the contents of nest boxes from which snake-like hisses emerge.     

Choosing suitable hosts: common cuckoos Cuculus canorus parasitize great reed warblers Acrocephalus arundinaceus of high quality

We investigated the hypothesis that the common cuckoo Cuculus canorus selects host pairs of good phenotypic quality. As there is some evidence that cuckoos may select hosts within a population non-randomly based on external cues reflecting their foster abilities, we predicted that great reed warbler Acrocephalus arundinaceus pairs parasitized by the cuckoo would exhibit higher quality than unparasitized ones. To test this assumption, we evaluated two different parameters indicating host quality: body condition and characteristics of host eggs. We found that parasitized females showed significantly better body condition than unparasitized ones, and the model showed that the probability of being parasitized by the cuckoos increased with increasing body condition. Moreover, the likelihood of being parasitized by a cuckoo within the great reed warbler population increased with decreasing colour variability within clutches: parasitized females allocated costly blue pigments to eggshells more equally compared with unparasitized ones. Our study revealed that cuckoos parasitize great reed warbler females of higher quality, as reflected in host body condition and egg colour characteristics. In highly mimetic systems, cuckoos may choose to parasitize hosts with eggs displaying low intraclutch variation, both because this leads to reduced rejection and because these hosts are of high quality.     

Climatic effects and phenological mismatch in cuckoo–host interactions: a role for host phenotypic plasticity in laying date?

Climatic effects on breeding phenology vary across organisms and therefore might promote a phenological mismatch in ecologically interacting species, including those engaged in coevolutionary interactions such as brood parasites and their hosts. Recent studies suggest that climatic induced changes in migration phenology may have mismatched cuckoos and their hosts in Europe. However, it is currently unknown whether cuckoo–host phenological mismatch results from different degrees of phenotypic plasticity or to different speeds of microevolutionary processes affecting hosts and parasites. Here we performed 1) cross‐sectional correlations between climate conditions and population level of phenological mismatch between the migratory brood parasite great spotted cuckoo Clamator glandarius and its main resident host in Europe, the magpie Pica pica; and 2) a longitudinal analysis to study within‐individual variation in breeding phenology for individual hosts experiencing different climate conditions over a period of nine years (2005–2013). Cross‐sectional analyses revealed independent and contrary effects of winter and spring temperature on magpie phenology: magpie hosts tend to breed earlier those years with lower February temperatures, however, high temperature in the first half of April spur individuals to lay eggs. Breeding phenology of cuckoos was tuned to that of their magpie host in time and duration. However, annual phenological mismatch between cuckoos and magpie hosts increased with NAO index and January temperature. Longitudinal analyses revealed high individual consistency in magpie host phenology, but a low influence of climate, suggesting that the climatic‐driven phenological mismatch between cuckoos and magpies at the population‐level cannot be explained by a host plastic response to climatic conditions.     

Social learning of a brood parasite by its host

Arms races between brood parasites and their hosts provide model systems for studying the evolutionary repercussions of species interactions. However, how naive hosts identify brood parasites as enemies remains poorly understood, despite its ecological and evolutionary significance. Here, we investigate whether young, cuckoo-naive superb fairy-wrens, Malurus cyaneus, can learn to recognize cuckoos as a threat through social transmission of information. Naive individuals were initially unresponsive to a cuckoo specimen, but after observing conspecifics mob a cuckoo, they made more whining and mobbing alarm calls, and spent more time physically mobbing the cuckoo. This is the first direct evidence that naive hosts can learn to identify brood parasites as enemies via social learning.     

Egg shape mimicry in parasitic cuckoos

Parasitic cuckoos lay their eggs in nests of host species. Rejection of cuckoo eggs by hosts has led to the evolution of egg mimicry by cuckoos, whereby their eggs mimic the colour and pattern of their host eggs to avoid egg recognition and rejection. There is also evidence of mimicry in egg size in some cuckoo–host systems, but currently it is unknown whether cuckoos can also mimic the egg shape of their hosts. In this study, we test whether there is evidence of mimicry in egg form (shape and size) in three species of Australian cuckoos: the fan‐tailed cuckoo Cacomantis flabelliformis, which exploits dome nesting hosts, the brush cuckoo Cacomantis variolosus, which exploits both dome and cup nesting hosts, and the pallid cuckoo Cuculus pallidus, which exploits cup nesting hosts. We found evidence of size mimicry and, for the first time, evidence of egg shape mimicry in two Australian cuckoo species (pallid cuckoo and brush cuckoo). Moreover, cuckoo–host egg similarity was higher for hosts with open nests than for hosts with closed nests. This finding fits well with theory, as it has been suggested that hosts with closed nests have more difficulty recognizing parasitic eggs than open nests, have lower rejection rates and thus exert lower selection for mimicry in cuckoos. This is the first evidence of mimicry in egg shape in a cuckoo–host system, suggesting that mimicry at different levels (size, shape, colour pattern) is evolving in concert. We also confirm the existence of egg size mimicry in cuckoo–host systems.     

Experimental study of alarm calls of the oriental tit (Parus minor) toward different predators and reactions they induce in nestlings

Anti-predatory strategies of birds are diverse and may include predator-specific alarm calls. For example, oriental tit (Parus minor) parents can distinguish snakes from other predators and produce snake-specific referential vocalizations ("jar" call) when a snake poses a threat to their nest. The “jar” call has a very specific function to induce fledging of nestlings close to fledging age. This reaction ensures nestlings' survival in natural encounters with snakes that are capable of entering nest cavities and kill entire broods. Sciurid rodents, like chipmunks, may pose a similar threat to cavity-nesting birds. We explored the hypothesis that parents use the fledging-inducing alarm vocalizations in this situation, because chipmunks, like snakes, can kill the brood upon entering the nest cavity. We compared alarm calls of parents toward two predators (chipmunk and snake) who pose a similar threat to the nestlings in a nest cavity, and toward an avian predator (Eurasian jay) who cannot enter nest cavities and poses no threat to the nestlings in a nest. Our results show that the vocal responses of oriental tits were different among the three predators. This suggests that the acoustic properties of vocal responses to predators are different between predators of a similar hunting strategy (nest-cavity entering). The playback of recorded vocal responses of parents to chipmunks did not trigger the fledging of old nestlings, whereas the vocalizations toward a snake did, as shown by earlier studies. Our study suggests that the vocal response of parents does not carry information about the ability of predators to enter the nest cavity and confirms the special status of alarm calls triggered by snakes.     

Age Differences in the Response of Willow Tits (Parus montanus) to Conspecific Alarm Calls

Predation is an important mortality factor in wintering birds. To counter this, birds produce alarm calls in the presence of predators which serve to warn conspecifics. In social hierarchical bird flocks, adults survive the winter better than juveniles and therefore survival strategies probably vary with social status. This study examined the differential responses to alarm calls by free-living willow tits, Parus montanus, in dominance-structured winter flocks in Finland. To explore the age-dependent differences in response to conspecific alarm calls, a series with three alarm calls was played to focal adults and juveniles while they sat in the middle section of a spruce branch. Immediately after the playback, juvenile willow tits moved more often, flew longer distances and changed branches more often than did adults. Previous mammal studies have shown that juveniles are more likely to flee than adults after hearing conspecific alarm calls. The current study demonstrates that similar age-dependent responses to conspecific alarm calls occur in birds also. These findings reflect an increased vulnerability to predators or lack of experience of young birds.     

Variation in and Meaning of Alarm Calls in a Social Desert Rodent Rhombomys opimus

The great gerbil (Rhombomys opimus), a social rodent that lives in family groups, emits three different alarm vocalizations in the presence of predators: a rhythmic call; a faster more intense call; and a single whistle. We tested the hypothesis that the alarm calls communicate risk of predation. We quantified the relationship between predator distance and type of alarm call via human approaches to gerbils. We also tested responses of focal adults in family groups to playback broadcasts of the different calls and controls of bird song and tape noise. Results showed that alarm calls were related to distance from a predator. Gerbils gave the rhythmic call when the predator was farthest away, the more intense call as the predator moved closer; and a short whistle when startled by a close approach of the predator. Gerbils stopped feeding and stood vigilant in a frozen alert posture in response to playbacks of all three alarm calls. They decreased non‐vigilant behavior to the alarm vocalizations more than to the controls and decreased non‐vigilant behavior significantly more in response to the intense alarm and whistle compared with the rhythmic alarm. We conclude that one function of gerbil alarm calls is to communicate response urgency to family members. The rhythmic alarm communicates danger at a distance, whereas the intense alarm and whistle signal the close approach of a predator.     

Rival imprinting: interspecifically cross-fostered tits defend their territories against heterospecific intruders

Failure to recognize conspecifics in social interactions such as mate choice and aggressive encounters will often result in reduced fitness. Studies on mate choice show that the ability to recognize conspecifics as mates is not universally present at birth, but often needs to be learned. In contrast, little is known about the ontogeny of intrasexual species recognition. To test whether learning influences the recognition of sexual rivals, we compared the aggressive response towards intruders of interspecifically cross-fostered individuals and controls reared by conspecific parents. We simulated territorial intrusion by presenting either a caged individual or playback song near the nest of breeding pairs of great tits, Parus major, and blue tits, P. caeruleus. Great tits reared by blue tit parents responded much more to blue tit stimuli than did great tit controls, and furthermore showed stronger responses to blue tit stimuli than to those of their own species. Blue tits reared by great tits responded much more to great tit stimuli than did blue tit controls. In contrast, blue tits cross-fostered to coal tits, P. ater, did not respond more to coal tits than did blue tit controls. There was a species difference in the response to conspecifics: blue tits cross-fostered to great tits responded more to conspecifics than did cross-fostered great tits. The results were similar for males and females. We conclude that learning influences intrasexual species recognition in these tits. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.