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.     

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.     

Ultraviolet reflectance of great spotted cuckoo eggs and egg discrimination by magpies

Hosts of obligate avian brood parasites use visual cues to distinguishbetween their own eggs and those of the parasite. Despite majordifferences between human and bird vision, most previous studieson cuckoo egg mimicry estimated color matching based on humancolor vision. Undetected by humans, ultraviolet reflectance(UVR) may play a previously ignored role for rejection behaviorin avian brood parasite systems. We explored this possibilityby manipulating UVR of great spotted cuckoo Clamator glandariuseggs and assessing the response of magpie Pica pica hosts. Wecoated cuckoo eggs with an ultraviolet (UV) light blocker thatreduced UVR but left the human visible reflectance (400–700nm) unaltered. The first control treatment also coated the eggsbut did not alter their reflectance. A second control groupof cuckoo eggs was maintained uncoated to control for handlingeffects on magpie discrimination. We artificially parasitizeda third of a breeding magpie population with each type of experimentalegg and studied the rejection of cuckoo eggs. We failed to findsignificant differences between rejection rate of cuckoo eggswith and without reduced reflectance in the UV region. Our resultsindicate that artificial reduction of UVR of cuckoo eggs doesnot affect the probability of ejection by magpie hosts.     

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.     

Host–parasite coevolution beyond the nestling stage? Mimicry of host fledglings by the specialist screaming cowbird

Egg mimicry by obligate avian brood parasites and host rejection of non-mimetic eggs are well-known textbook examples of host-parasite coevolution. By contrast, reciprocal adaptations and counteradaptations beyond the egg stage in brood parasites and their hosts have received less attention. The screaming cowbird (Molothrus rufoaxillaris) is a specialist obligate brood parasite whose fledglings look identical to those of its primary host, the baywing (Agelaioides badius). Such a resemblance has been proposed as an adaptation in response to host discrimination against odd-looking young, but evidence supporting this idea is scarce. Here, we examined this hypothesis by comparing the survival rates of young screaming cowbirds and non-mimetic shiny cowbirds (Molothrus bonariensis) cross-fostered to baywing nests and quantifying the similarity in plumage colour and begging calls between host and cowbird fledglings. Shiny cowbirds suffered higher post-fledging mortality rates (83%) than screaming cowbirds (0%) owing to host rejection. Visual modelling revealed that screaming cowbirds, but not shiny cowbirds, were indistinguishable from host young in plumage colour. Similarly, screaming cowbirds matched baywings' begging calls more closely than shiny cowbirds. Our results strongly support the occurrence of host fledgling mimicry in screaming cowbirds and suggest a role of visual and vocal cues in fledgling discrimination by baywings.     

Hosts of avian brood parasites have evolved egg signatures with elevated information content

Hosts of brood-parasitic birds must distinguish their own eggs from parasitic mimics, or pay the cost of mistakenly raising a foreign chick. Egg discrimination is easier when different host females of the same species each lay visually distinctive eggs (egg ‘signatures’), which helps to foil mimicry by parasites. Here, we ask whether brood parasitism is associated with lower levels of correlation between different egg traits in hosts, making individual host signatures more distinctive and informative. We used entropy as an index of the potential information content encoded by nine aspects of colour, pattern and luminance of eggs of different species in two African bird families (Cisticolidae parasitized by cuckoo finches Anomalospiza imberbis, and Ploceidae by diederik cuckoos Chrysococcyx caprius). Parasitized species showed consistently higher entropy in egg traits than did related, unparasitized species. Decomposing entropy into two variation components revealed that this was mainly driven by parasitized species having lower levels of correlation between different egg traits, rather than higher overall levels of variation in each individual egg trait. This suggests that irrespective of the constraints that might operate on individual egg traits, hosts can further improve their defensive ‘signatures'' by arranging suites of egg traits into unpredictable combinations.     

Egg phenotype differentiation in sympatric cuckoo Cuculus canorus gentes

The brood parasitic common cuckoo Cuculus canorus consists of gentes, which typically parasitize only a single host species whose eggs they often mimic. Where multiple cuckoo gentes co‐exist in sympatry, we may expect variable but generally poorer mimicry because of host switches or inter‐gens gene flow via males if these also contribute to egg phenotypes. Here, we investigated egg trait differentiation and mimicry in three cuckoo gentes parasitizing great reed warblers Acrocephalus arundinaceus, marsh warblers Acrocephalus palustris and corn buntings Miliaria calandra breeding in close sympatry in partially overlapping habitat types. The three cuckoo gentes showed a remarkable degree of mimicry to their three host species in some but not all egg features, including egg size, a hitherto largely ignored feature of egg mimicry. Egg phenotype matching for both background and spot colours as well as for egg size has been maintained in close sympatry despite the possibility for gene flow.     

Brood parasites lay eggs matching the appearance of host clutches

Interspecific brood parasitism represents a prime example of the coevolutionary arms race where each party has evolved strategies in response to the other. Here, we investigated whether common cuckoos (Cuculus canorus) actively select nests within a host population to match the egg appearance of a particular host clutch. To achieve this goal, we quantified the degree of egg matching using the avian vision modelling approach. Randomization tests revealed that cuckoo eggs in naturally parasitized nests showed lower chromatic contrast to host eggs than those assigned randomly to other nests with egg-laying date similar to naturally parasitized clutches. Moreover, egg matching in terms of chromaticity was better in naturally parasitized nests than it would be in the nests of the nearest active non-parasitized neighbour. However, there was no indication of matching in achromatic spectral characteristics whatsoever. Thus, our results clearly indicate that cuckoos select certain host nests to increase matching of their own eggs with host clutches, but only in chromatic characteristics. Our results suggest that the ability of cuckoos to actively choose host nests based on the eggshell appearance imposes a strong selection pressure on host egg recognition.     

Evidence for aggressive mimicry in an adult brood parasitic bird,and generalized defences in its host

Mimicry of a harmless model (aggressive mimicry) is used by egg, chick and fledgling brood parasites that resemble the host''s own eggs, chicks and fledglings. However, aggressive mimicry may also evolve in adult brood parasites, to avoid attack from hosts and/or manipulate their perception of parasitism risk. We tested the hypothesis that female cuckoo finches (Anomalospiza imberbis) are aggressive mimics of female Euplectes weavers, such as the harmless, abundant and sympatric southern red bishop (Euplectes orix). We show that female cuckoo finch plumage colour and pattern more closely resembled those of Euplectes weavers (putative models) than Vidua finches (closest relatives); that their tawny-flanked prinia (Prinia subflava) hosts were equally aggressive towards female cuckoo finches and southern red bishops, and more aggressive to both than to their male counterparts; and that prinias were equally likely to reject an egg after seeing a female cuckoo finch or bishop, and more likely to do so than after seeing a male bishop near their nest. This is, to our knowledge, the first quantitative evidence for aggressive mimicry in an adult bird, and suggests that host–parasite coevolution can select for aggressive mimicry by avian brood parasites, and counter-defences by hosts, at all stages of the reproductive cycle.     

Avian colour perception predicts behavioural responses to experimental brood parasitism in chaffinches

Hosts of cuckoos have evolved defences allowing them to discriminate and reject parasite eggs. Mechanisms of discrimination are mostly visually mediated, and have been studied using approaches that do not account for what the receiver (i.e. host) actually can discriminate. Here, for the first time we apply a perceptual model of colour discrimination to study behavioural responses to natural variation in parasite egg appearance in chaffinches Fringilla coelebs. Discrimination of parasite eggs gradually increased with increasing differences in chromatic contrasts as perceived by birds between parasite and host eggs. These results confirm that colour differences of the eggs as perceived by birds are important integral parts of a matching signal used by chaffinch hosts.     

鸟类巢寄生伤害理论的进化

鸟类巢寄生的寄主无论是成乌还是雏鸟,对宿主都是极具伤害性的,因为它们降低了宿主的生育力,然而,无论是在寄主种内还是种间,其伤害性的差异变化很大。综述了以往对这种伤害性差异的各种解释,以往的解释在很大程度上集中在伤害性所带来的利益。认为寄主的伤害性行为可以像病原体的伤害性一样进行分类,伤害性在为寄主带来利益的同时,也伴随着代价,所以,由病原体伤害性进化研究衍生而来的平衡假说,适用于解释鸟类巢寄生伤害理论的进化。