Differences in the nestling begging calls of hosts and host-races of the common cuckoo, Cuculus canorus

We compared nestling begging calls of four hosts (reed warbler, Acrocephalus scirpaceus; great reed warbler, A. arundinaceus; dunnock, Prunella modularis; and meadow pipit, Anthus pratensis) and the respective host-races of the common cuckoo. Note structure varied between host species, but not between cuckoo host-races, so cuckoos did not vary their call note structure to match that of their hosts' chicks. Call rate increased with age, but there were marked differences between both host species and cuckoo host-races. Dunnock-cuckoos called more rapidly than reed warbler-cuckoos despite growing at the same rate. We suggest this difference reflects how cuckoos tune into the way these host species respond to begging signals from their own young, because dunnock chicks called much more rapidly than reed warbler chicks. Great reed warbler-cuckoos called at a lower rate than reed warbler-cuckoos when young, but at a greater rate when older than 8 days. This could also result from the cuckoo chicks tuning into differences in the way these hosts respond to begging signals. However, great reed warbler-cuckoos grew at a faster rate than the other cuckoo host-races, so they may also call faster to demand higher provisioning rates from this larger host. To test these hypotheses critically, data are needed on how the different host species integrate visual and vocal begging signals from their own broods. We discuss how differences in cuckoo begging might develop, given that cuckoo host-races are restricted to female cuckoo lineages. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

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.     

Breeding success of common cuckoos Cuculus canorus parasitising four sympatric species of Acrocephalus warblers

We investigated the level of parasitism, egg mimicry and breeding success of cuckoos parasitising four sympatric species of Acrocephalus warblers in southern Moravia, Czech Republic. The parasitism rate was highest in the marsh warbler Acrocephalus palustris (44.8%) followed by great reed warbler A. arundinaceus (33.8%), sedge warbler A. schoenobaenus (26.5%) and reed warbler A. scirpaceus (11.6%). Although the cuckoo eggs showed a high level of mimicry the eggs of the marsh warbler this host species rejected 72% of the cuckoo eggs, resulting in a cuckoo breeding success of only 4.3%. Cuckoo eggs laid in great reed warbler and reed warbler nests showed a similar hatching success, but the cuckoo chicks survived better in great reed warbler nests, resulting in a breeding success of 30.4%, as compared to 16.4% in nests of the reed warbler. The relationship between the level of parasitism, host rejection of cuckoo eggs, cuckoo chick survival and breeding success is discussed for the four host species.     

Continuous Variation Rather than Specialization in the Egg Phenotypes of Cuckoos (Cuculus canorus) Parasitizing Two Sympatric Reed Warbler Species

The evolution of brood parasitism has long attracted considerable attention among behavioural ecologists, especially in the common cuckoo system. Common cuckoos (Cuculus canorus) are obligatory brood parasites, laying eggs in nests of passerines and specializing on specific host species. Specialized races of cuckoos are genetically distinct. Often in a given area, cuckoos encounter multiple hosts showing substantial variation in egg morphology. Exploiting different hosts should lead to egg-phenotype specialization in cuckoos to match egg phenotypes of the hosts. Here we test this assumption using a wild population of two sympatrically occurring host species: the great reed warbler (Acrocephalus arundinaceus) and reed warbler (A. scirpaceus). Using colour spectrophotometry, egg shell dynamometry and egg size measurements, we studied egg morphologies of cuckoos parasitizing these two hosts. In spite of observing clear differences between host egg phenotypes, we found no clear differences in cuckoo egg morphologies. Interestingly, although chromatically cuckoo eggs were more similar to reed warbler eggs, after taking into account achromatic differences, cuckoo eggs seemed to be equally similar to both host species. We hypothesize that such pattern may represent an initial stage of an averaging strategy of cuckoos, that – instead of specializing for specific hosts or exploiting only one host – adapt to multiple hosts.     

Nestling discrimination without recognition: a possible defence mechanism for hosts towards cuckoo parasitism?

One of the great evolutionary puzzles is why hosts of parasitic birds discriminate finely against alien eggs, but almost never discriminate against parasitic chicks. A theoretical model has shown that an adaptive host response to alien eggs can be based on learning. However, learned nestling discrimination is too costly to be favoured by selection in hosts of evicting parasites, such as the European cuckoo (Cuculus canorus). Indeed, parasitic chick rejection has never been reported for any European cuckoo host species. As learned nestling discrimination is maladaptive, one can expect that a viable alternative for hosts would be to use discrimination mechanisms not involving learning and/or recognition. We suggest that hosts may starve and desert cuckoo chicks that require higher amounts of food than an average host brood at fledging (i.e. feeding rates to a parasite are outside the normal range of host behaviour in unparasitized nests). Our observations of the reed warbler (Acrocephalus scirpaceus) at parasitized nests indicate that such behaviour could possibly work in this host species.     

The common cuckoo Cuculus canorus is not locally adapted to its reed warbler Acrocephalus scirpaceus host

The obligate avian brood parasitic common cuckoo Cuculus canorus comprises different strains of females that specialize on particular host species by laying eggs of a constant type that often mimics those of the host. Whether cuckoos are locally adapted for mimicking populations of the hosts on which they are specialized has never been investigated. In this study, we first explored the possibility of local adaptation in cuckoo egg mimicry over a geographical mosaic of selection exerted by one of its main European hosts, the reed warbler Acrocephalus scirpaceus. Secondly, we investigated whether cuckoos inhabiting reed warbler populations with a broad number of alternative suitable hosts at hand were less locally adapted. Cuckoo eggs showed different degrees of mimicry to different reed warbler populations. However, cuckoo eggs did not match the egg phenotypes of their local host population better than eggs of other host populations, indicating that cuckoos were not locally adapted for mimicry on reed warblers. Interestingly, cuckoos exploiting reed warblers in populations with a relatively larger number of co-occurring cuckoo gentes showed lower than average levels of local adaptation in egg volume. Our results suggest that cuckoo local adaptation might be prevented when different cuckoo populations exploit more or fewer different host species, with gene flow or frequent host switches breaking down local adaptation where many host races co-occur.     

Rapid increase in cuckoo egg matching in a recently parasitized reed warbler population

Parasitic cuckoos lay eggs that mimic those of their hosts, and such close phenotypic matching may arise from coevolutionary interactions between parasite and host. However, cuckoos may also explicitly choose hosts in a way that increases degree of matching between eggs of cuckoos and parasites, with female preference for specific host phenotypes increasing the degree of matching. We tested for temporal change in degree of matching between eggs of the parasitic European cuckoo (Cuculus canorus) and its reed warbler (Acrocephalus scirpaceus) host during 24 consecutive years in a recently parasitized reed warbler population. Cuckoo-host egg matching in an ultraviolet-brownness component yielding most of the chromatic variance of eggs improved during the study period. Improved matching was not due to changes in cuckoo egg phenotype. Cuckoo eggs matched host eggs for ultraviolet-brownness within nests irrespective of duration of sympatry. Ultraviolet-brownness of cuckoo eggs was similar to that of reed warbler eggs at parasitized nests, but differed from that of reed warbler eggs at unparasitized nests. These findings provide tentative support for the cuckoo preference hypothesis suggesting that cuckoo-host egg matching could partially be due to cuckoo females selecting host nests based on the appearance of their eggs.     

Eviction behaviour of the common cuckoo Cuculus canorus chicks

We studied the eviction behaviour of common cuckoo Cuculus canorus chicks by video recording at nests of great reed warblers Acrocephalus arundinaceus and reed warblers Acrocephalus scirpaceus . There were no significant differences in hatching mass and age at first eviction between cuckoos reared by either host. However, mass at eviction had a significant effect on the timing of first eviction event. No significant difference in time required to evict was found between serial intranest eviction events for cuckoos raised by either host. However, "great reed warbler" cuckoos evicted significantly quicker than "reed warbler" cuckoos during particular eviction events. A majority (70%) of "reed warbler" cuckoos evicted during the day, while most "great reed warbler" cuckoos evicted nocturnally (63%). We did not find any effect of the temperature inside or outside the nest on eviction behaviour. Both "great reed warbler" and "reed warbler" cuckoos evicted regardless the fact whether a parent was absent or present at the nest. Interestingly, individual cuckoos were consistent in their eviction behaviour relative to host presence or absence; particular cuckoo chick evicted only when the parents were present or absent from the nest.     

An exceptionally high diversity of hoverflies (Syrphidae) in the food of the reed warbler (Acrocephalus scirpaceus)

Despite being considered a classical example of protective Batesian mimicry hoverflies (Syrphidae) are known to be preyed upon by various passerines. The aim of the present study was to examine in detail food brought by reed warblers Acrocephalus scirpaceus to their nests to better understand the importance of hoverflies in the diet of small passerines. Using neck collars, 273 food samples containing 8,545 food items delivered to reed warbler and parasitic common cuckoo Cuculus canorus nestlings in warbler nests were recorded. The study was conducted during three breeding seasons in South Moravia, Czech Republic. An unusually high diversity of hoverflies was found — 27 species, including Mesembrius peregrinus (critically endangered species in the Czech Republic) and Mallota cimbiciformis (endangered species) — a new taxon to the Czech Republic. This indicates that nestling diet analyses may provide not only information on avian foraging behaviour but also important faunistic data. Thus, without the detailed identification to species level of material from foraging behaviour studies valuable scientific information may be lost. Overall dominance of Syrphidae was 3.7%, the most common species being Episyrphus balteatus (55.7%, n = 318). However, this number seriously underestimates the importance of hoverflies in the diet of reed warblers as hoverflies are one of the largest prey taken by warblers. Both larvae and pupae were rare, imagines strongly dominating (92.7%). Both specific wasp mimics (e.g., Chrysotoxum verrali) and bee mimics (e.g., Eristalis spp.) were not avoided by foraging reed warblers. The presence of a parasitic cuckoo chick did not affect host foraging behaviour with respect to overall dominance of hoverflies in the diet (warbler 3.3%, cuckoo 3.8%).     

The importance of nest cleaning in egg rejection behaviour of great reed warblers Acrocephalus arandinaceas

We tested the importance of nest cleaning in egg rejection behaviour of the great reed warbler Acrocephalus arundinaceus in a highly parasitised population in which about 64% of nests are parasitised by the common cuckoo Cuculus canorus . Three types of objects of the same weight, texture and colour but with different shapes (dummy cuckoo eggs, sticks and disks) were placed into great reed warbler nests. We investigated the response of hosts in two stages of breeding: pre-incubation when the risk of brood parasitism is high, and during incubation when the risk of parasitism is low. The dummy cuckoo eggs were rejected less often than the other objects in both breeding stages, although we did not find any difference in the frequency of rejection between pre-incubation and incubation. We integrate these results into current views on the evolution of host–parasite interactions, and propose a hierarchical concept to understand egg rejection behaviour: (1) hosts reject all non-egg shaped objects as a general cleaning mechanism; (2) adaptations for the hosts' ability to recognise their own eggs allows them to distinguish these eggs from similar objects and parasitic eggs.     

Great reed warbler Acrocephalus arundinaceus and reed warbler Acrocephalus scirpaceus respond differently to cuckoo dummy at the nest

A cuckoo Cuculus canorus dummy was exposed at 24 nests of great reed warbler Acrocephalus arundinaceus (GRW) and 34 nests of reed warbler Acrocephalus scirpaceus (RW) during the egg-laying stage. The eight GRW pairs attacked the cuckoo directly, striking the dummy, but such a behaviour was not recorded in RWs. Also, other behavioural measures (closest distance from the model, duration of distress calls and number of excitement calls) indicated a lower level of defence by RWs compared to GRWs. In the study area, the parasitism rate was much lower in GRWs (1.7% of nests) than in RWs (11.3%). We suggest that one of the reasons for the lower level of cuckoo parasitism on GRWs is its stronger nest defence and hence higher risk of injury or even death for the cuckoo during egg dumping.     

REED WARBLER HOSTS FINE‐TUNE THEIR DEFENSES TO TRACK THREE DECADES OF CUCKOO DECLINE

Interactions between avian hosts and brood parasites can provide a model for how animals adapt to a changing world. Reed warbler (Acrocephalus scirpaceus) hosts employ costly defenses to combat parasitism by common cuckoos (Cuculus canorus). During the past three decades cuckoos have declined markedly across England, reducing parasitism at our study site (Wicken Fen) from 24% of reed warbler nests in 1985 to 1% in 2012. Here we show with experiments that host mobbing and egg rejection defenses have tracked this decline in local parasitism risk: the proportion of reed warbler pairs mobbing adult cuckoos (assessed by responses to cuckoo mounts and models) has declined from 90% to 38%, and the proportion rejecting nonmimetic cuckoo eggs (assessed by responses to model eggs) has declined from 61% to 11%. This is despite no change in response to other nest enemies or mimetic model eggs. Individual variation in both defenses is predicted by parasitism risk during the host's egg‐laying period. Furthermore, the response of our study population to temporal variation in parasitism risk can also explain spatial variation in egg rejection behavior in other populations across Europe. We suggest that spatial and temporal variation in parasitism risk has led to the evolution of plasticity in reed warbler defenses.     

Eggshell characteristics and yolk composition in the common cuckoo Cuculus canorus: are they adapted to brood parasitism?

The developmental rate of cuckoo embryos and their hatching size is greater than that of host species, which may require more nutrient resources in the egg and more intensive gas exchange during development. In the present study, we compared various egg characteristics of a brood parasite, the common cuckoo Cuculus canorus, and its frequent host, the great reed warbler Acrocephalus arundinaceus. As maternally‐derived testosterone is known to enhance growth rate of embryos and hatchlings, cuckoo eggs are expected to contain higher concentration of testosterone than host eggs. In addition, we expected higher concentration of antioxidants in cuckoo eggs to protect embryos from oxidative stress associated with accelerated growth. Our results showed that cuckoo eggs had thicker shells and higher pore density than great reed warbler eggs. Yolk was significantly heavier in cuckoo eggs and contained higher concentrations of carotenoids and vitamin E, however, yolk androgen and immunoglobulin concentrations were lower in cuckoo eggs as compared to great reed warbler eggs. We also examined whether eggshell colour was associated to egg quality, and detected a positive association between blue‐green chroma and yolk antioxidant concentration in both species, suggesting that eggshell colour reflects the antioxidant investment of the female into the eggs. Our results suggest that cuckoo females increase the size, growth rate and competitive ability of their young by providing them with more nutrients and more dietary antioxidants for embryonic development, and not through elevated yolk testosterone or antibody levels. In addition, increased porosity of cuckoo eggshells may allow embryos to develop more rapidly because of a greater capacity of gas exchange.     

Learning fine-tunes a specific response of nestlings to the parental alarm calls of their own species

Parent birds often give alarm calls when a predator approaches their nest. However, it is not clear whether these alarms function to warn nestlings, nor is it known whether nestling responses are species-specific. The parental alarms of reed warblers, Acrocephalus scirpaceus ("churr"), dunnocks, Prunella modularis ("tseep"), and robins, Erithacus rubecula ("seee") are very different. Playback experiments revealed that nestlings of all three species ceased begging only in response to conspecific alarm calls. These differences between species in response are not simply a product of differences in raising environment, because when newly hatched dunnocks and robins were cross-fostered to nests of the other two species, they did not develop a response to their foster species' alarms. Instead, they still responded specifically to their own species' alarms. However, their response was less strong than that of nestlings raised normally by their own species. We suggest that, as in song development, a neural template enables nestlings to recognize features of their own species' signals from a background of irrelevant sounds, but learning then fine-tunes the response to reduce recognition errors.     

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.     

Dynamic egg color mimicry

Evolutionary hypotheses regarding the function of eggshell phenotypes, from solar protection through mimicry, have implicitly assumed that eggshell appearance remains static throughout the laying and incubation periods. However, recent research demonstrates that egg coloration changes over relatively short, biologically relevant timescales. Here, we provide the first evidence that such changes impact brood parasite–host eggshell color mimicry during the incubation stage. First, we use long‐term data to establish how rapidly the Acrocephalus arundinaceus Linnaeus (great reed warbler) responded to natural parasitic eggs laid by the Cuculus canorus Linnaeus (common cuckoo). Most hosts rejected parasitic eggs just prior to clutch completion, but the host response period extended well into incubation (~10 days after clutch completion). Using reflectance spectrometry and visual modeling, we demonstrate that eggshell coloration in the great reed warbler and its brood parasite, the common cuckoo, changes rapidly, and the extent of eggshell color mimicry shifts dynamically over the host response period. Specifically, 4 days after being laid, the host should notice achromatic color changes to both cuckoo and warbler eggs, while chromatic color changes would be noticeable after 8 days. Furthermore, we demonstrate that the perceived match between host and cuckoo eggshell color worsened over the incubation period. These findings have important implications for parasite–host coevolution dynamics, because host egg discrimination may be aided by disparate temporal color changes in host and parasite eggs.     

Habitat-dependent call divergence in the common cuckoo: is it a potential signal for assortative mating?

The common cuckoo (Cuculus canorus) is an obligate brood parasite that mimics the eggs of its hosts. The host-specific egg pattern is thought to be inherited matrilinearly, creating female-only host-specific races. Males are thought not to be adapted to their host and they maintain the species by mating arbitrarily with respect to host specialization of females. However, recent results suggest that male cuckoos may also show host-specific adaptations and these may require assortative mating with respect to host. The calls males produce on the breeding grounds could provide a potential mechanism for assortative mating. We tested whether male cuckoo calls differ more between nearby populations that parasitize different hosts than between distant populations that parasitize the same host. We recorded the calls of geographically distant pairs of populations in Hungary, with each pair consisting of a forest population and a nearby reed bed population. Each habitat is characterized by one main host species for the common cuckoo. Our results show that calls of distant cuckoo populations from the same habitat type are more similar to each other than they are to those of nearby populations from a different habitat. These results suggest that cuckoo calls differ sufficiently to allow recognition of habitat-specific individuals.     

Responses of great reed warblers Acrocephalus arundinaceus to experimental brood parasitism: the effects of a cuckoo Cuculus canorus dummy and egg mimicry

Egg rejection behaviour towards parasitic eggs was studied in a great reed warbler Acrocephalus arundinaceus population in central Hungary, which was heavily (about 65%) parasitised by the common cuckoo Cuculus canorus . Clutches were experimentally parasitised during the egg-laying period with artificial, moderately mimetic cuckoo eggs or with conspecific eggs that were good mimics of the hosts' eggs. Great reed warblers rejected 76.2% of the artificial cuckoo eggs, mainly by ejection, but accepted most of the conspecific eggs (87.5%). Cuckoo eggs in naturally parasitised clutches were rejected at a lower rate (32%). When, in addition to the egg mimicry experiments, a stuffed cuckoo was placed near the nest, accompanied by the recording of a female cuckoo call, hosts' rejection rate of the artificial cuckoo egg increased from 76% to 96%. The sight of the cuckoo, on the other hand, did not influence host's rejection behaviour when a conspecific egg was used in the experiment. A stuffed collared dove Streptopelia decaocto , accompanied by its call, was used as a control, and did not cause any increased rejection. Great reed warblers were more aggressive towards the cuckoo than to the dove dummy. When the cuckoo eggs in naturally parasitised clutches were exchanged with artificial cuckoo eggs, we observed no increase in the rejection rate. We conclude that great reed warblers in our heavily parasitised population are capable of detecting brood parasitism in their clutch by identifying the parasitic egg. The efficiency of this identification depends mainly on the mimicry of the foreign egg. The sight of the cuckoo at the nest may increase rejection rate by stimulus summation, and this conditional effect is mainly affected by the degree of mimicry of the parasitic egg.     

Competition with a host nestling for parental provisioning imposes recoverable costs on parasitic cuckoo chick's growth

Chicks of the brood parasitic common cuckoo (Cuculus canorus) typically monopolize host parental care by evicting all eggs and nestmates from the nest. To assess the benefits of parasitic eviction behaviour throughout the full nestling period, we generated mixed broods of one cuckoo and one great reed warbler (Acrocephalus arundinaceus) to study how hosts divide care between own and parasitic young. We also recorded parental provisioning behaviour at nests of singleton host nestlings or singleton cuckoo chicks. Host parents fed the three types of broods with similar-sized food items. The mass of the cuckoo chicks was significantly reduced in mixed broods relative to singleton cuckoos. Yet, after the host chick fledged from mixed broods, at about 10-12 days, cuckoo chicks in mixed broods grew faster and appeared to have compensated for the growth costs of prior cohabitation by fledging at similar weights and ages compared to singleton cuckoo chicks. These results are contrary to suggestions that chick competition in mixed broods of cuckoos and hosts causes an irrecoverable cost for the developing brood parasite. Flexibility in cuckoos' growth dynamics may provide a general benefit to ecological uncertainty regarding the realized successes, failures, and costs of nestmate eviction strategies of brood parasites.     

Shared parental care is costly for nestlings of common cuckoos and their great reed warbler hosts

Obligate avian brood parasitism typically involves one of 2strategies: parasite chicks are either 1) virulent and evictall other eggs and nest mates to be raised alone or 2) moretolerant and share foster parental care with host chicks forsome or the entirety of the nestling period. We studied theconsequences of experimentally forced mixed broods of age-matchedone common cuckoo (Cuculus canorus) and 2 great reed warbler(Acrocephalus arundinaceus) chicks. In these broods, both cuckooand host chicks grew slower than did either individual cuckoosor great reed warblers in broods of 1 parasite or 3 host chicks,respectively. Video records showed that in mixed broods, cuckoochicks received feedings less frequently than the 33% predictedby chance at 4 days of age but parental food allocations increasedto chance levels at 8 days of age. The consistent patterns oflower growth rates arose even though chicks in broods of 1 parasiteand 2 hosts received the largest prey items per feeding. Inaddition, several other measures of parental provisioning alsodid not predict species and brood-specific differences in nestlinggrowth rates across the different treatments. However, variationin begging displays and its specific costs on host and parasitechicks in the different nest treatments were not quantifiedin this study. We conclude that young of nest mate–evictorcommon cuckoos benefit from the sole occupancy of host nestsin part owing to an initial competitive disadvantage for parentalcare in broods with age-matched great reed warbler chicks.