Antagonistic antiparasite defenses: nest defense and egg rejection in the magpie host of the great spotted cuckoo

Brood parasites dramatically reduce the reproductive successof their hosts, which therefore have developed defenses againstbrood parasites. The first line of defense is protecting thenest against adult parasites. When the parasite has successfullyparasitized a host nest, some hosts are able to recognize andreject the eggs of the brood parasite, which constitutes the secondline of defense. Both defense tactics are costly and would be counteractedby brood parasites. While a failure in nest defense implies successfulparasitism and therefore great reduction of reproductive successof hosts, a host that recognizes parasitic eggs has the opportunityto reduce the effect of parasitism by removing the parasiticegg. We hypothesized that, when nest defense is counteractedby the brood parasite, hosts that recognize cuckoo eggs shoulddefend their nests at a lower level than nonrecognizers becausethe former also recognize adult cuckoos. Magpie (Pica pica) hoststhat rejected model eggs of the brood parasitic great spottedcuckoo (Clamator glandarius) showed lower levels of nest defensewhen exposed to a great spotted cuckoo than when exposed toa nest predator (a carrion crow Corvus corone). Moreover, magpiesrejecting cuckoo eggs showed lower levels of nest defense againstgreat spotted cuckoos than nonrecognizer magpies, whereas differencesin levels of defense disappeared when exposed to a carrion crow.These results suggest that hosts specialize in antiparasitedefense and that different kinds of defense are antagonistically expressed.We suggest that nest-defense mechanisms are ancestral, whereasegg recognition and rejection is a subsequent stage in the coevolutionaryprocess. However, host recognition ability will not be expressedwhen brood parasites break this second line of defense.     

Evolution of host egg mimicry in a brood parasite, the great spotted cuckoo

Brood parasitism in birds is one of the best examples of coevolutionary interactions in vertebrates. Coevolution between hosts and parasites is assumed to occur because the parasite imposes strong selection pressures on its hosts, reducing their fitness and thereby favouring counter-adaptations (e.g. egg rejection) which, in turn, select for parasite resistance (e.g. egg mimicry). Great spotted cuckoos ( Clamator glandarius ) are usually considered a brood parasite with eggs almost perfectly mimicking those of their host, the magpie ( Pica pica ). However, Cl. glandarius also exploits South African hosts with very different eggs, both in colour and size, while the Cl. glandarius eggs are similar to those laid in nests of European hosts. Here, we used spectrophotometric techniques for the first time to quantify mimicry of parasitic eggs for eight different host species. We found: (1) non-significant differences in appearance of Cl. glandarius eggs laid in nests of different host species, although eggs laid in South Africa and Europe differed significantly; (2) contrary to the general assumption that Cl. glandarius eggs better mimic those of the main host in Europe ( P. pica ), Cl. glandarius eggs more closely resembled those of the azure-winged magpie ( Cyanopica cyana ), a potential host in which there is no evidence of recent parasitism; (3) the appearance of Cl. glandarius eggs was not significantly related to the appearance of host eggs. We discuss three possible reasons why Cl. glandarius eggs resemble eggs of some of their hosts. We suggest that colouration of Cl. glandarius eggs is an apomorphic trait, and that variation between eggs laid in South African and European host nests is due to genetic isolation among these populations and not due to variation in colouration of host eggs.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 551–563.     

Is egg-damaging behavior by great spotted cuckoos an accident or an adaptation?

Adult great spotted cuckoos Clamator glandarius damage the eggsof their magpie Pica pica host without removing them from thenest or eating them but by producing the death of the embryo.Observations as well as experiments were used to test severalpredictions of two different possibilities: great spotted cuckooegg-damaging behavior is a parasitic tactic resulting froma direct selection process (the adaptation hypothesis), oregg damage is caused by thick-shelled cuckoo eggs which evolvedto avoid breakage during rapid laying (the nonadaptation hypothesis).Previously, we provided experimental evidence that egg damageincreased the breeding success of cuckoos when they laid lateduring the laying sequence of the magpie. However, when theylaid early, egg-damaging behavior did not increase cuckoo breedingsuccess, contrary to the adaptation hypothesis. In an experimental study, when we simulated laying behavior by the great spottedcuckoo, we found that (1) the number of damaged magpie eggswas significantly lower than in natural parasitism, and (2)whereas in the experimental manipulations the number of damagedeggs did not depend on the number of magpie eggs, in natural parasitism, the number of damaged eggs increased with clutchsize of the magpie. These results support the predictions ofthe adaptation hypothesis, implying that egg damage is notan incidental consequence of rapid egg laying, but an adaptation.     

Micro-evolutionary change and population dynamics of a brood parasite and its primary host: the intermittent arms race hypothesis

A long-term study of the interactions between a brood parasite, the great spotted cuckoo Clamator glandarius, and its primary host the magpie Pica pica, demonstrated local changes in the distribution of both magpies and cuckoos and a rapid increase of rejection of both mimetic and non-mimetic model eggs by the host. In rich areas, magpies improved three of their defensive mechanisms: nest density and breeding synchrony increased dramatically and rejection rate of cuckoo eggs increased more slowly. A stepwise multiple regression analysis showed that parasitism rate decreased as host density increased and cuckoo density decreased. A logistic regression analysis indicated that the probability of changes in magpie nest density in the study plots was significantly affected by the density of magpie nests during the previous year (positively) and the rejection rate of mimetic model eggs (negatively). These results are consistent with a hypothesis (the intermittent arms race hypothesis) of spatially structured cyclic changes in parasitism. During periods of parasitism, host defences continuously improve, and as a consequence, the fitness gains for parasites decrease. When host defences against parasites reach a high level, dispersing parasites have a selective advantage if they are able to emigrate to areas of low resistance. Once parasites have left an area hosts will lose their defensive adaptations due to their cost in the absence of parasitism. The scene is then set for re-colonization by great spotted cuckoos. Received: 7 May 1998 / Accepted: 24 August 1998     

Change in host rejection behavior mediated by the predatory behavior of its brood parasite

Passerine hosts of parasitic cuckoos usually vary in their abilityto discriminate and reject cuckoo eggs. Costs of discriminationand rejection errors have been invoked to explain the maintenanceof this within-population variability. Recently, enforcementof acceptance by parasites has been identified as a rejectioncost in the magpie (Pica pica) and its brood parasite, the greatspotted cuckoo (Clamator glandarius). Previous experimentalwork has shown that rejecter magpies suffer from increased nestpredation by the great spotted cuckoo. Cuckoo predatory behavioris supposed to confer a selective advantage to the parasitebecause magpies experiencing a reproductive failure may providea second opportunity for the cuckoo to parasitize a replacementclutch. This hypothesis implicitly assumes that magpies modulatetheir propensity to reject parasite eggs as a function of previousexperience. We tested this hypothesis in a magpie populationbreeding in study plots varying in parasitism rate. Magpie pairs thatwere experimentally parasitized and had their nests depredated,after their rejection behavior had been assessed, changed theirbehavior from rejection to acceptance. The change in host behaviorwas prominent in study plots with high levels of parasitism,but not in plots with rare or no cuckoo parasitism. We discussthree possible explanations for these differences, concludingthat in study plots with a high density of cuckoos, the probability fora rejecter magpie nest of being revisited and depredated bya cuckoo is high, particularly for replacement clutches, and,therefore, the cost for magpies of rejecting a cuckoo egg ina replacement clutch is increased. Moreover, in areas with highlevels of host defense (low parasitism rate), the probabilityof parasitism and predation of rejecter-magpie nests by thecuckoo is reduced in both first and replacement clutches. Therefore,rejecter magpies in such areas should not change their rejectionbehavior in replacement clutches.     

Spatial patterns of egg laying and multiple parasitism in a brood parasite: a non-territorial system in the great spotted cuckoo (Clamator glandarius)

We analysed the spatial and temporal pattern of egg laying in great spotted cuckoo females using microsatellite typing to determine parentage of the eggs and nestlings found in host (magpie) nests. The results showed that there were no exclusive laying territories in the study area. Cases of multiparasitism could be due to single females laying two or more eggs in a nest, or to several females using the same nest. In the latter case multiparasitism was due to a shortage of available host nests. We argue that the need for very large laying areas and the likely small cost of sharing parental care for chicks make the costs of defending territories higher than the benefits, which has constrained the evolution of territoriality in this species. Received: 16 March 1998 / Accepted: 15 June 1998     

Manipulation of hunger levels affects great spotted cuckoo and magpie host nestlings differently

Brood parasitic nestlings usually exhibit an exaggerated begging behaviour, which is mainly attributed to reduced inclusive fitness costs since they typically share the nest with unrelated individuals. However, energetic costs also constrain begging expression and accordingly a relation between food requirements and intensity of begging behaviour could also exist in brood parasites, just as in nesting bird species. Here, we tested this hypothesis in the great spotted cuckoo Clamator glandarius and its main host, the magpie Pica pica, by studying the effect of an appetite enhancer, cyproheptadine hydrochloride, on nestling provisioning and development (size, body mass and cell‐mediated immune response). To study nestling provisioning, neck‐collars were meticulously placed around nestling necks allowing normal respiration but avoiding the ingestion of food delivered by adult magpies during ca 2.5 h. Loss in body mass during neck‐collar trials was used as a proxy for energetic begging costs, while the amount of food received during these trials and growth during the whole nestling period were used as variables reflecting short‐ and long‐term effects of the experimental treatment. During neck‐collar trials, we found that experimental nestlings of both species received more food than control nestlings. However, experimental magpies, but not cuckoos, lost more body mass than control nestlings. These results suggest a short‐term beneficial effect of an escalated begging behaviour in both species that would be energetically cheaper for cuckoos than for magpies. We found positive long‐term effects of the appetite enhancer only in magpies (in terms of tarsus and wing length at fledging, but not in terms of immune response and body mass); suggesting that exaggerated begging would be beneficial for hosts only. We discuss the possible effect of begging behaviour on the risk of predation and on inclusive fitness, but also the possibility that our results may be explained by some kind of limitation in the capability of food assimilation by parasitic species.     

A quantitative trait locus for recognition of foreign eggs in the host of a brood parasite

Avian brood parasites reduce the reproductive output of their hosts and thereby select for defence mechanisms such as ejection of parasitic eggs. Such defence mechanisms simultaneously select for counter-defences in brood parasites, causing a coevolutionary arms race. Although coevolutionary models assume that defences and counter-defences are genetically influenced, this has never been demonstrated for brood parasites. Here, we give strong evidence for genetic differences between ejector and nonejectors, which could allow the study of such host defence at the genetic level, as well as studies of maintenance of genetic variation in defences. Briefly, we found that magpies, that are the main host of the great spotted cuckoo in Europe, have alleles of one microsatellite locus (Ase64) that segregate between accepters and rejecters of experimental parasitic eggs. Furthermore, differences in ejection rate among host populations exploited by the brood parasite covaried significantly with the genetic distance for this locus.     

Telomere dynamics in parasitic great spotted cuckoos and their magpie hosts

Although little is known on the impact of environment on telomere length dynamics, it has been suggested to be affected by stress, lifestyle and/or life‐history strategies of animals. We here compared telomere dynamics in erythrocytes of hatchlings and fledglings of the brood parasite great spotted cuckoos (Clamator glandarius) and of magpies (Pica pica), their main host in Europe. In magpie chicks, telomere length decreased from hatching to fledging, whereas no significant change in telomere length of great spotted cuckoo chicks was found. Moreover, we found interspecific differences in the association between laying date and telomere shortening. Interspecific differences in telomere shortening were interpreted as a consequence of differences in lifestyle and life‐history characteristics of magpies and great spotted cuckoos. In comparison with magpies, cuckoos experience reduced sibling competition and higher access to resources and, consequently, lower stressful environmental conditions during the nestling phase. These characteristics also explain the associations between telomere attrition and environmental conditions (i.e. laying date) for magpies and the absence of association for great spotted cuckoos. These results therefore fit expectations on telomere dynamics derived from interspecific differences in lifestyle and life history of brood parasites and their bird hosts.     

Coevolution of an avian host and its parasitic cuckoo

Abstract We use a quantitative genetic model to examine the coevolution of host and cuckoo egg characters (termed "size" as a proxy for general appearance), host discrimination, and host and cuckoo population dynamics. A host decides whether to discard an egg using a comparison of the sizes of the eggs in her nest, which changes as host and cuckoo eggs evolve. Specifically, we assume that the probability that she discards the largest egg in her nest depends on how much larger it is than the second largest egg. This decision rule (i.e., the acceptable difference in egg sizes) also evolves, changing both the chance of successful rejection of a cuckoo egg in parasitized nests and the chance of mistaken rejection of a host egg in both parasitized and unparasitized nests. We find a stable equilibrium for coexistence of the host and cuckoo where there is cuckoo egg mimicry, evolutionary displacement of the host egg away from the cuckoo egg phenotype, and host discrimination against unusual eggs. Both host discrimination and host egg displacement are fairly weak at the equilibrium. Cuckoo egg mimicry, although imperfect, usually evolves more extensively and quickly than the responses of the host. Our model provides evidence for both the evolutionary equilibrium and evolutionary lag hypotheses of host acceptance of parasitic eggs.     

Great spotted cuckoos respond earlier to the arrival of feeding foster parents and perform less erroneous begging when hungry than their magpie host nest‐mates

In many bird species, parents usually feed the first nestling that starts to beg before its nest‐mates. The pressure to avoid missed feeds could trigger nestlings to perform in erroneous begging in absence of parents, which has the same costs as begging in the presence of parents but without any reward. So, nestlings should try to minimize both erroneous begging and missed feeds simultaneously. The threshold to start begging is predicted to be lower for hungry nestlings and for nestlings that are unrelated to their nest‐mates, because they suffer lower inclusive fitness costs when depriving nest‐mates of food. In line with this idea, we found that brood parasitic great spotted cuckoo nestlings responded sooner than their magpie nest‐mates when an adult arrived to the nest. Under laboratory conditions, nestlings of both species rarely incurred in erroneous begging when food was abundant, but under conditions of restricted food, magpie nestlings increased erroneous begging while cuckoo nestlings did not. Highly conspicuous begging in cuckoos results in an increased predation risk, which could have resulted in stronger selection pressures on cuckoos to avoid erroneous begging, probably resulting in better developed perceptual abilities, allowing cuckoos to perform better than their host nest‐mates.     

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.     

Cuckoo parasitism and productivity in different magpie subpopulations predict frequencies of the 457bp allele: a mosaic of coevolution at a small geographic scale

The level of defense against great spotted cuckoo (Clamator glandarius) parasitism in different European populations of magpie (Pica pica) depends on selection pressures due to parasitism and gene flow between populations, which suggests the existence of coevolutionary hot spots within a European metapopulation. A mosaic of coevolution is theoretically possible at small geographical scales and with strong gene flow, because, among other reasons, plots may differ in productivity (i.e., reproductive success of hosts in the absence of parasitism) and defensive genotypes theoretically should be more common in plots of high productivity. Here, we tested this prediction by exploring the relationship between parasitism rate, level of defense against parasitism (estimated as both rejection rate and the frequency of the 457bp microsatellite allele associated with foreign egg rejection in magpies), and some variables related to the productivity (average laying date, clutch size, and number of hatchlings per nest) of magpies breeding in different subpopulations. We found that both estimates of defensive ability (egg rejection rate and frequency of the 457bp allele) covaried significantly with between-plot differences in probability of parasitism, laying date, and number of hatchlings per nest. Moreover, the parasitism rate was larger in more productive plots. These results confirm the existence of a mosaic of coevolution at a very local geographical scale, and the association between laying date and number of hatchlings with variables related to defensive ability and the selection pressure arising from parasitism supports the prediction of coevolutionary gradients in relation to host productivity.     

Bacterial diversity at the cloaca relates to an immune response in magpie Pica pica and to body condition of great spotted cuckoo Clamator glandarius nestlings

Diversity of the gut bacterial community is of prime importance for optimal food digestion and, therefore, for nutritional condition of avian nestlings. Consequently, bacterial community should be considered as a predictor of the future survival and recruitment of young birds. To explore this hypothesis, we studied the cloacal microbiota, by using RISA procedure, in two avian species sharing environmental conditions during growth, the avian brood parasitic great spotted cuckoo Clamator glandarius , and their main host in Europe, the magpie Pica pica . As estimates of phenotypic condition of nestlings we studied two nutrition-dependent traits, the immune response to an innocuous antigen (phytohemagglutinin), and the residuals of body mass on tarsus and wing length of nestlings. According to the hypothesis, we found significant relationships between microbial diversity and nestling phenotypic traits related to probability of recruitment. Briefly, both magpie and cuckoo nestlings having more similar microbial diversity were also those with similar immune response and body condition index respectively. Our results show a possible association between bacterial communities and variables related to the probability of post-fledging survival and recruitment of birds, as well as possible reasons explaining magpie-cuckoo differences in the nutritionally conditioned variables better associated with their bacterial diversity.     

Innate development of acoustic signals for host parent–offspring recognition in the brood‐parasitic Screaming Cowbird Molothrus rufoaxillaris

Young birds communicate their need to parents through complex begging displays that include visual and acoustic cues. Nestlings of interspecific brood parasites must ‘tune’ into these communication channels to secure parental care from their hosts. Various studies show that parasitic nestlings can effectively manipulate host parental behaviour through their begging calls, but how these manipulative acoustic signals develop in growing parasites remains poorly understood. We investigated the influence of social experience on begging call development in a host‐specialist brood parasite, the Screaming Cowbird Molothrus rufoaxillaris. Screaming Cowbird nestlings look and sound similar to those of the primary host, the Greyish Baywing Agelaioides badius. This resemblance is likely to be adaptive because Baywings discriminate against fledglings unlike their own and provision nests at higher rates in response to Baywing‐like begging calls than to non‐mimetic begging calls. By means of cross‐fostering and playback experiments, we tested whether the acoustic cues that elicit recognition by Baywings develop innately in Screaming Cowbird nestlings or are acquired through social experience with host parents or nest mates. Our results suggest that begging call structure was partially modulated by experience because Baywing‐reared Screaming Cowbird and host nestlings were acoustically more similar as age increased, whereas acoustic similarity between cross‐fostered and Baywing‐reared Screaming Cowbird nestlings decreased from 4–5 to 8–10 days of age. Cross‐fostered Screaming Cowbirds developed begging calls of lower minimum frequency and broader bandwidth than those of Baywing‐reared Screaming Cowbirds by the age of 8–10 days. Despite the observed differences in begging call structure, however, adult Baywings responded similarly to begging calls of 8‐ to 10‐day‐old cross‐fostered and Baywing‐reared Screaming Cowbirds, suggesting that these were functionally equivalent from the host's perspective. These findings support the idea that, although rearing environment can influence certain begging call parameters, the acoustic cues that serve for offspring recognition by Baywings develop in young Screaming Cowbirds independently of social experience.     

Host sexual selection and cuckoo parasitism: an analysis of nest size in sympatric and allopatric magpie Pica pica populations parasitized by the great spotted cuckoo Clamator glandarius

Magpies (Pica pica) build large nests that are the target of sexual selection, since males of early breeding pairs provide many sticks for nests and females mated to such males enjoy a material fitness benefit in terms of better quality territory and parental care of superior quality. Great spotted cuckoos (Clamator glandarius) preferentially parasitize large magpie nests and sexual selection for large nests is thus opposed by natural selection due to brood parasitism. Consistent with the hypothesized opposing selection pressures, in a comparative analysis of 14 magpie populations in Europe we found that nest volume was consistently smaller in sympatry than in allopatry with the great spotted cuckoo, in particular in areas with a high parasitism rate and high rates of rejection of mimetic model cuckoo eggs. These observations are consistent with the suggestion that magpies have evolved a smaller nest size in areas where cuckoos have exerted strong selection pressures on them in the recent past.     

Persistence of egg recognition in the absence of cuckoo brood parasitism: pattern and mechanism

Broad ecological shifts can render previously adaptive traits nonfunctional. It is an open question as to how and how quickly nonfunctional traits decay once the selective pressures that favored them are removed. The village weaverbird (Ploceus cucullatus) avoids brood parasitism by rejecting foreign eggs. African populations have evolved high levels of within-clutch uniformity as well as individual distinctiveness in egg color and spotting, a combination that facilitates identification of foreign eggs. In a companion study, I showed that these adaptations in egg appearance declined following introductions of weavers into habitats devoid of egg-mimicking brood parasites. Here, I use experimental parasitism in two ancestral and two introduced populations to test for changes in egg rejection behavior while controlling for changes in egg appearance. Introduced populations reject foreign eggs less frequently, but the ability of source and introduced populations to reject foreign eggs does not differ after controlling for the evolution of egg color and spotting. Therefore, egg rejection behavior in introduced populations of the village weaver has been compromised by changes in egg appearance, but there has been no significant decline in the birds' ability to recognize foreign eggs. This result reconciles earlier studies on this system and provides insights into the ways behavior can change over generations, especially in the context of recognition systems and the avoidance of brood parasitism.     

The spatial habitat structure of host populations explains the pattern of rejection behavior in hosts and parasitic adaptations in cuckoos

In this article we present tentative support for predictionsderived from a spatial habitat structure hypothesis arguingthat common cuckoos Cuculus canorus, the most common obligatebrood parasite in Europe, only breed in areas where they haveaccess to vantage points in trees. Thus, species in which somepopulations breed near trees while other populations breed farther from trees have a different cuckoo—host population dynamicthan species in which all populations always breed in the vicinityof trees. Parasitism rate, mimicry of brood parasite eggs withthose of the hosts, and rejection behavior of hosts varieswith the host breeding habitat. Cuckoos are best adapted toexploit species in which some populations breed near trees while other populations breed in open areas because such hosts arenot always accessible to cuckoos, and thus gene flow amongunparasitized and parasitized populations delays the evolutionof host adaptations. Adaptive behavior in cuckoos as well asin their hosts can be predicted from the spatial habitat structurehypothesis.