Eavesdropping cuckoos: further insights on great spotted cuckoo preference by magpie nests and egg colour

Reproductive success of brood parasites largely depends on appropriate host selection and, although the use of inadvertent social information emitted by hosts may be of selective advantage for cuckoos, this possibility has rarely been experimentally tested. Here, we manipulated nest size and clutch colouration of magpies (Pica pica), the main host of great spotted cuckoos (Clamator glandarius). These phenotypic traits may potentially reveal information about magpie territory and/or parental quality and could hence influence the cuckoo’s choice of host nests. Experimentally reduced magpie nests suffered higher predation rate, and prevalence of cuckoo parasitism was higher in magpie nests with the densest roofs, which suggests a direct advantage for great spotted cuckoos choosing this type of magpie nest. Colouration of magpie clutches was manipulated by adding one artificial egg (blue or cream colouration) at the beginning of the egg-laying period. We found that host nests holding an experimental cream egg experienced a higher prevalence of cuckoo parasitism than those holding a blue-coloured egg. Results from these two experiments suggest that great spotted cuckoos cue on magpie nest characteristics and the appearance of eggs to decide parasitism, and confirm, for the first time, the ability of cuckoos to distinguish between eggs of different colours within the nest of their hosts. Several hypothetical scenarios explaining these results are discussed.     

Brood parasitism is associated with increased bacterial contamination of host eggs: bacterial loads of host and parasitic eggs

Factors related to bacterial environment of nests are of primary interest for understanding the causes of embryo infection and the evolution of antimicrobial defensive traits in birds. Nest visitors such as parasites could act as vectors for bacteria and/or affect the hygienic conditions of nests and hence influence the nest bacterial environment. In the present study, we explored some predictions of this hypothetical scenario in the great spotted cuckoo (Clamator glandarius)–magpie (Pica pica) system of brood parasitism. Great spotted cuckoos visit the nests of their magpie hosts and frequently damage some of the host eggs when laying eggs or on subsequent visits. Therefore, it represents a good system for testing the effect of nest visitors on the bacterial environment of nests. In accordance with this hypothesis, we found that the bacterial load of magpie eggshells was greater in parasitized nests, which may suggest that brood parasitism increases the probability of bacterial infection of magpie eggs. Moreover, comparisons of bacterial loads of cuckoo and magpie eggs revealed that: (1) cuckoo eggshells harboured lower bacterial densities than those of their magpie hosts in the same nests and (2) the prevalence of bacteria inside unhatched eggs was higher for magpies than for great spotted cuckoos. These interspecific differences were predicted because brood parasitic eggs (but not host eggs) always experience the bacterial environments of parasitized nests. Therefore, the results obtained in the present study suggest that parasitic eggs are better adapted to environments with a high risk of bacterial contamination than those of their magpie hosts. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 836–848.     

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.     

Egg rejection by Iberian azure-winged magpies Cyanopica cyanus in the absence of brood parasitism

The Iberian azure-winged magpie Cyanopica cyanus shows a remarkable ability to discriminate against great spotted cuckoo Clamator glandarius eggs. Here, I studied whether egg recognition in this species could be a derived feature resulting from intra-specific brood parasitism. Azure-winged magpies showed a very high level of discrimination and rejection of great spotted cuckoo models (73.7%), and of conspecific eggs (42.8%), even when no evidence of great spotted cuckoo or conspecific brood parasitism has been found in the population. Azure-winged magpie discriminated more readily than magpies, the current favourite host of the great spotted cuckoo. The high rejection rate of conspecific eggs by the azure-winged magpie suggests that it is quite possible that egg discrimination in this species evolved in response to conspecific brood parasitism rather than to cuckoo parasitism.     

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.     

Synchronization of laying by great spotted cuckoos and recognition ability of magpies

Brood parasites rely entirely on the parental care of host species to raise the parasitic nestlings until independence. The reproductive success of avian brood parasites depends on finding host nests at a suitable stage (i.e. during egg laying) for parasitism and weakly defensive (i.e. non‐ejector) hosts. Finding appropriate nests for parasitism may, however, vary depending on ecological conditions, including parasite abundance in the area, which also varies from one year to another and therefore may influence coevolutionary relationships between brood parasites and their hosts. In this scenario, we explored: 1) the degree of laying synchronization between great spotted cuckoos Clamator glandarius and magpies Pica pica during two breeding seasons, which varied in the level of selection pressure due to brood parasitism (i.e. parasitism rate); 2) magpie responses to natural parasitism in the pre‐laying period and successfulness of parasitic eggs laid at this stage; and 3) magpie responses to experimental parasitism performed at different breeding stages. We found that, during the year of higher parasitism rate, there was an increase in the percentage of parasitic eggs laid before magpies started laying. However, the synchronization of laying was poor both years regardless of the differences in the parasitism rate. The ejection rate was significantly higher during the pre‐egg‐laying and the post‐hatching stages than during the laying stage, and hatching success of parasitic eggs laid during the pre‐egg‐laying stage was zero. Thus, non‐synchronized parasitic eggs are wasted and therefore poor synchronization should be penalized by natural selection. We discuss four different hypotheses explaining poor synchronization.     

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     

Brood-parasite interactions between great spotted cuckoos and magpies: a model system for studying coevolutionary relationships

Brood parasitism is one of the systems where coevolutionary processes have received the most research. Here, we review experiments that suggest a coevolutionary process between the great spotted cuckoo (Clamator glandarius) and its magpie (Pica pica) host. We focus on different stages of establishment of the relationship, from cuckoos selecting individual hosts and hosts defending their nests from adult cuckoos, to the ability of magpies to detect cuckoo eggs in their nests. Novel coevolutionary insights emerge from our synthesis of the literature, including how the evolution of "Mafia" behaviour in cuckoos does not necessarily inhibit the evolution of host recognition and rejection of cuckoo offspring, and how different populations of black-billed magpies in Europe have evolved specific host traits (e.g. nest and clutch size) as a result of interactions with the great spotted cuckoo. Finally, the results of the synthesis reveal the importance of using a meta-population approach when studying coevolution. This is especially relevant in those cases where gene flow among populations with different degrees of brood parasitism explains patterns of coexistence between defensive and non-defensive host phenotypes. We propose the use of a meta-population approach to distinguish between the "evolutionary equilibrium" hypothesis and the "evolutionary lag" hypothesis.     

Evolution of tolerance by magpies to brood parasitism by great spotted cuckoos

Hosts may use two different strategies to ameliorate negative effects of a given parasite burden: resistance or tolerance. Although both resistance and tolerance of parasitism should evolve as a consequence of selection pressures owing to parasitism, the study of evolutionary patterns of tolerance has traditionally been neglected by animal biologists. Here, we explore geographical covariation between tolerance of magpies (Pica pica) and brood parasitism by the great spotted cuckoo (Clamator glandarius) in nine different sympatric populations. We estimated tolerance as the slope of the regression of number of magpie fledglings (i.e. host fitness) on number of cuckoo eggs laid in non-depredated nests (which broadly equals parasite burden). We also estimated prevalence of parasitism and level of host resistance (i.e. rejection rates of mimetic model eggs) in these nine populations. In accordance with the hypothetical role of tolerance in the coevolutionary process between magpies and cuckoos we found geographical variation in tolerance estimates that positively covaried with prevalence of parasitism. Levels of resistance and tolerance were not associated, possibly suggesting the lack of a trade-off between the two kinds of defences against great spotted cuckoo parasitism for magpies. We discuss the results in the framework of a mosaic of coevolutionary interactions along the geographical distribution of magpies and great spotted cuckoos for which we found evidence that tolerance plays a major role.     

Great Spotted Cuckoos Frequently Lay Their Eggs While Their Magpie Host is Incubating

Species that suffer from brood parasitism face a considerable reduction in their fitness which selects for the evolution of host defences. To prevent parasitism, hosts can mob or attack brood parasites when they approach the host nest and block the access to the nest by sitting on the clutch. In turn, as a counter‐adaptation, brood parasites evolved secretive behaviours near their host nests. Here, we have studied great spotted cuckoo (Clamator glandarius) egg‐laying behaviour and defence by their magpie (Pica pica) hosts inside the nest using continuous video recordings. We have found several surprising results that contradict some general assumptions. The most important is that most (71%) of the parasitic events by cuckoo females are completed while the magpie females are incubating. By staying in the nest, magpies force cuckoo females to lay their egg facing the high risk of being attacked by the incubating magpie (attack occurred in all but one of the events, n = 15). During these attacks, magpies pecked the cuckoo violently, but could never effectively avoid parasitism. These novel observations expand the sequence of adaptations and counter‐adaptations in the arms race between brood parasites and their hosts during the pre‐laying and laying periods.