Egg removal by cuckoos forces hosts to accept parasite eggs

Many avian brood parasites remove one or more host eggs before laying their own eggs in the host nest. Various hypotheses have been proposed to explain the adaptive significance of this behaviour, but none of them provides an adequate explanation. Here we provide a new hypothesis for explaining why a parasite removes host eggs before laying its own. In this study, we attempted to answer this question by constructing a mathematical model that focused on the changes in host decision making according to reduced clutch size as a consequence of egg removal by parasites. We assume that a host selects one of the following two options to maximise the number of its own chicks: trying to eject a suspicious egg from the nest (trying‐to‐eject) or acceptance without trying to eject the egg (acceptance). The option selected depends on the number of eggs in the nest. Our model provides a new explanation for egg removal behaviour by showing that the host should select trying‐to‐eject if there is a large number of eggs in the nest but acceptance with a small number of eggs. This is because the relative payoff for a host that selects trying‐to‐eject decreases with the number of eggs in the nest. Therefore, parasites benefit by removing the host egg because this behaviour reduces the number of eggs in the nest, thereby increasing the probability of their own eggs being accepted. Thus, hosts have evolved egg ejection to combat brood parasites, but it may also have facilitated the evolution of egg removal by parasites. This hypothesis may also apply to brood parasitic species that do not eject host chicks. In addition, this hypothesis may explain other parasitic behaviours, such as egg damaging and egg puncturing, which lead to reductions in the host clutch size.     

Relative reproductive success of female moorhens using conditional strategies of brood parasitism and parental care

In a population of moorhens (Gallinula chloropus), at least27% of netting females laid one or more eggs in a neighbor'snest Females laid parasitically under three conditions: 56%of parasitic eggs were from nesting females that preceded layinga dutch in their own nest by a parasitic laying bout, 19% werefrom females whose nests were depredated before clutch completionand that laid the following egg parasiticaDy, and 25% were froma small number of females without territories, "non-nesting"parasites, that each laid a series of parasitic eggs. Clutchsizes varied greatly between females, but nesting females eachlaid a consistent clutch size both within and between seasonsfor a given mate and territory. Nesting females that employeda dual strategy of brood parasitism and parental care producedextra eggs that they laid in the nests of neighbors before layinga dutch in their own nests. Two out of ten females whose dutchesI experimentally removed during the laying period were successfullyinduced to lay their next egg in the nest of a neighbor. Nestingfemales that laid parasitically selected their hosts opportunisticallyfrom among the nests dosest to their territories. An experimentin which parasitic eggs were removed and hosts left to rearonly their own young showed that parasites did not choose hoststhat were better parents than pairs with contemporary neststhat were not parasitized. Females that only laid parasiticaDywithin a given season timed their parasitic laying bouts poorlyand achieved no reproductive success. Parasitic young rarelyfledged, and the mean seasonal reproductive success of nestingbrood parasites did not differ from that of nonparasitic females.However, the variance in reproductive success of nesting broodparasites was significantly higher than that of nonparasiticfemales.     

Relatedness and spatial proximity as determinants of host–parasite interactions in the brood parasitic Barrow's goldeneye (Bucephala islandica)

Recent studies, which have found evidence for kin-biased egg donation, have sparked interest in re-assessing the parasitic nature of conspecific brood parasitism (CBP). Since host–parasite kinship is essential for mutual benefits to arise from CBP, we explored the role of relatedness in determining the behaviour of conspecific nest parasites and their hosts in nesting female Barrow's goldeneyes ( Bucephala islandica ), a duck in which CBP is common. The results revealed that the amount of parasitism increased with host–parasite relatedness, the effect of which was independent of geographical proximity of host and parasite nests. Proximity per se was also positively associated with the amount of parasitism. Furthermore, while hosts appeared to reduce their clutch size as a response to the presence of parasitic eggs, the magnitude of host clutch reduction also tended to increase with increasing relatedness to the parasite. Hence, our results indicate that both relatedness and spatial proximity are important determinants of CBP, and that host clutch reduction may be an adaptation to nest parasitism, modulated by host–parasite relatedness. Taken together, the results provide a demonstration that relatedness influences host and parasite behaviour in Barrow's goldeneyes, resulting in kin-biased egg donation.     

Intraspecific nest parasitism in the European starling Sturnus vulgaris

Biochemical genetic markers were used along with conventional methods (abnormal laying sequence/clutch size, unusual egg shape/pigmentation) to identify intraspecific nest parasitism at two British nestbox colonies of the European starling. Between 11 and 37% of first clutches were parasitized during 1977–1979. Parasitic females probably comprised all of the following categories: (1) paired females contesting a nestbox occupied by another pair; (2) previously paired females who had laid a clutch but had been unsuccessful; (3) unpaired females who had copulated with males that already had a mate and nest site; and (4) ‘professional’ nest parasites who distributed at lest some of their eggs in one or more nests other than their own. Although parasitized nests had higher clutch sizes, parasitism led to fewer host young fledging per egg laid, mainly through the eviction of eggs and subsequent nest desertion. Number of parasitic young fledged per egg laid was highest when eggs were laid synchronously with the host, when host clutches were larger, or a smaller number of parasite eggs were added to a nest, thus favouring parasites that distribute their eggs amongst a number of nests. A greater pressure on nest sites may have accounted for the higher levels of parasitism at the Aberdeen colony and for the greater number of parasite eggs laid in a nest. Although most parasitic female starlings appeared to be much less successful than non-parasitic ones, nest parasitism in the starling might evolve directly when one or more of the following advantages are present. (1) There are no constraints on the number of eggs a female may lay but there are constraints on the number of young she may feed adequately. (2) Female survival is increased by having fewer or no eggs/young to care for. (3) Current feeding conditions favour the survival of more young than would be produced by the most common clutch size. Intraspecific nest parasitism is considered to be a first stage in the evolution of interspecific nest parasitism.     

To eject or to abandon? Life history traits of hosts and parasites interact to influence the fitness payoffs of alternative anti‐parasite strategies

Hosts either tolerate avian brood parasitism or reject it by ejecting parasitic eggs, as seen in most rejecter hosts of common cuckoos, Cuculus canorus, or by abandoning parasitized clutches, as seen in most rejecter hosts of brown‐headed cowbirds, Molothrus ater. What explains consistent variation between alternative rejection behaviours of hosts within the same species and across species when exposed to different types of parasites? Life history theory predicts that when parasites decrease the fitness of host offspring, but not the future reproductive success of host adults, optimal clutch size should decrease. Consistent with this prediction, evolutionarily old cowbird hosts, but not cuckoo hosts, have lower clutch sizes than related rarely‐ or newly parasitized species. We constructed a mathematical model to calculate the fitness payoffs of egg ejector vs. nest abandoner hosts to determine if various aspects of host life history traits and brood parasites’ virulence on adult and young host fitness differentially influence the payoffs of alternative host defences. These calculations showed that in general egg ejection was a superior anti‐parasite strategy to nest abandonment. Yet, increasing parasitism rates and increasing fitness values of hosts’ eggs in both currently parasitized and future replacement nests led to switch points in fitness payoffs in favour of nest abandonment. Nonetheless, nest abandonment became selectively more favourable only at lower clutch sizes and only when hosts faced parasitism by a cowbird‐ rather than a cuckoo‐type brood parasite. We suggest that, in addition to evolutionary lag and gape‐size limitation, our estimated fitness differences based on life history trait variation provide new insights for the consistent differences observed in the anti‐parasite rejection strategies between many cuckoo‐ and cowbird‐hosts.     

Errors in egg-laying by female Common Cuckoo Cuculus canorus in nests of its common host

Dozens of studies have documented that brood parasites are well adapted to a brood parasitic lifestyle but not all parasitism events are successful. Co-evolution between brood parasites and their hosts is a dynamic process so it is reasonable to expect that a female brood parasite may commit errors during egg deposition by laying her eggs outside the laying period of the host, with consequent impacts on her fitness. Using an extensive dataset from a long-term study, we evaluated egg-laying patterns and errors related to the timing of egg-laying in the Common Cuckoo Cuculus canorus (hereafter ‘Cuckoo’). Specifically, we tested whether the Cuckoo avoids laying before or on the day of host clutch initiation to reduce the risk of rejection of parasitic eggs, whether laying errors will be more frequent in periods with a lack of active host nests, and whether the laying errors will be more frequent in periods with intense Cuckoo parasitism and a consequent lack of suitable host nests. We found that about one-third of Cuckoo eggs were laid on the host clutch initiation day or 1 day before, and the percentage of Cuckoo eggs laid decreased thereafter. Surprisingly, the probability of Cuckoo egg acceptance by the hosts was not affected by the egg-laying stage of the host clutch. Errors in the timing of egg-laying with fatal consequences (i.e. those precluding Cuckoo hatching because of laying in incubated or deserted clutches) were recorded in about 5% of cases. Only laying date of a Cuckoo egg had a significant effect on the probability of errors, which increased during the breeding season. This may be related to the higher number of deserted and incubated host nests at the site at the end of the breeding season. Errors in egg-laying may be attributed to young and inexperienced females but also impaired body condition or intraspecific competition may cause this behaviour. Future studies, which will test these possible explanations, will help to understand better the mechanism of co-evolutionary arms races and differences between host specialist and generalist brood parasites in various host–parasite systems.     

Brood parasitism,female condition and clutch reduction in the common eider Somateria mollisima

Conspecific brood parasitism (CBP) is an alternative reproductive tactic found in many animals with parental care. Parasitizing females lay eggs in the nests of other females (hosts) of the same species, which incubate and raise both their own and the foreign offspring. The causes and consequences of CBP are debated. Using albumen fingerprinting of eggs for accurately detecting parasitism, we here analyse its relation to female condition and clutch size in High Arctic common eiders Somateria mollissima borealis. Among 166 clutches in a Svalbard colony, 31 (19%) contained eggs from more than one female, and 40 of 670 eggs (6%) were parasitic. In 6 cases an active nest with egg(s) was taken over by another female. Many suitable nest sites were unoccupied, indicating that CBP and nest takeover are reproductive tactics, not only consequences of nest site shortage. Similarity in body mass between female categories suggests that condition does not determine whether a nesting female becomes parasitised. There was no evidence of low condition in parasites: egg size was similar in hosts and parasites, and parasitism was equally frequent early and late in the laying season. Meta‐analysis of this and 3 other eider studies shows that there is a cost of being parasitised in this precocial species: host females laid on average 7% fewer eggs than other females.     

FREQUENCY-DEPENDENT FITNESS CONSEQUENCES OF INTRASPECIFIC NEST PARASITISM IN SNOW GEESE

The reproductive efficiency, defined as the number of breeding recruits produced per egg laid; of intraspecific nest parasites; of hosts in parasitized nests; and of unparasitized nesting females, was measured for 14 years for lesser snow geese Anser caerulescens caerulescens nesting near Churchill, Manitoba, Canada. Relative efficiencies were 0.71–0.88, 0.91, and 1.0 for eggs of parasites, hosts, and unparasitized birds, respectively. Differences in the hatching probabilities of the three classes of eggs produced the efficiency differences. Parasitic success was limited by the parasites' failure to place more eggs than expected by chance into nests at the appropriate time relative to host incubation. Host nesting success was lower when more than one parasitic egg was added to the clutch. No differences in gosling survival and breeding recruitment probabilities were detected among any categories of goslings. Thus, hatching parasitic young are at no disadvantage relative to parental young, and there is no support for the hypothesis that increased success of host young at later stages of reproduction might offset negative effects at the egg stage. The hatching efficiency of parasitic eggs declined more rapidly than that of parental eggs as the parasitism rate increased. Efficiencies were similar when 3–4% of the eggs laid per year were parasitic, but relative parasitic efficiency was significantly lower when the parasitism rate was 8–9% or more. Using ancillary information and assumptions about the fecundity, viability, and behavioral flexibility of parasitic and parental females, we conclude that intraspecific nest parasitism could compete with nesting as a reproductive strategy in this population. The conditional use of parasitism by a large component of the population in certain years, however, combined with negative-frequency dependent success, limits the potential spread of a purely parasitic strategy in this population.     

Colony kin structure and host‐parasite relatedness in the barnacle goose

Conspecific brood parasitism (CBP), females laying eggs in the nest of other ‘host’ females of the same species, is a common alternative reproductive tactic among birds. For hosts there are likely costs of incubating and rearing foreign offspring, but costs may be low in species with precocial chicks such as waterfowl, among which CBP is common. Waterfowl show strong female natal philopatry, and spatial relatedness among females may influence the evolution of CBP. Here we investigate fine‐scale kin structure in a Baltic colony of barnacle geese, Branta leucopsis, estimating female spatial relatedness using protein fingerprints of egg albumen, and testing the performance of this estimator in known mother‐daughter pairs. Relatedness was significantly higher between neighbour females (nesting ≤ 40 metres from each other) than between females nesting farther apart, but there was no further distance trend in relatedness. This pattern may be explained by earlier observations of females nesting close to their mother or brood sisters, even when far from the birth nest. Hosts and parasites were on average not more closely related than neighbour females. In 25 of 35 sampled parasitized nests, parasitic eggs were laid after the host female finished laying, too late to develop and hatch. Timely parasites, laying eggs in the host’s laying sequence, had similar relatedness to hosts as that between neighbours. Females laying late parasitic eggs tended to be less related to the host, but not significantly so. Our results suggest that CBP in barnacle geese might represent different tactical life‐history responses.     

Experimental Shifts in Intraclutch Egg Color Variation Do Not Affect Egg Rejection in a Host of a Non-Egg-Mimetic Avian Brood Parasite

Avian brood parasites lay their eggs in the nests of other birds, and impose the costs associated with rearing parasitic young onto these hosts. Many hosts of brood parasites defend against parasitism by removing foreign eggs from the nest. In systems where parasitic eggs mimic host eggs in coloration and patterning, extensive intraclutch variation in egg appearances may impair the host’s ability to recognize and reject parasitic eggs, but experimental investigation of this effect has produced conflicting results. The cognitive mechanism by which hosts recognize parasitic eggs may vary across brood parasite hosts, and this may explain variation in experimental outcome across studies investigating egg rejection in hosts of egg-mimicking brood parasites. In contrast, for hosts of non-egg-mimetic parasites, intraclutch egg color variation is not predicted to co-vary with foreign egg rejection, irrespective of cognitive mechanism. Here we tested for effects of intraclutch egg color variation in a host of nonmimetic brood parasite by manipulating egg color in American robins (Turdus migratorius), hosts of brown-headed cowbirds (Molothrus ater). We recorded robins’ behavioral responses to simulated cowbird parasitism in nests where color variation was artificially enhanced or reduced. We also quantified egg color variation within and between unmanipulated robin clutches as perceived by robins themselves using spectrophotometric measures and avian visual modeling. In unmanipulated nests, egg color varied more between than within robin clutches. As predicted, however, manipulation of color variation did not affect rejection rates. Overall, our results best support the scenario wherein egg rejection is the outcome of selective pressure by a nonmimetic brood parasite, because robins are efficient rejecters of foreign eggs, irrespective of the color variation within their own clutch.     

Costs and response to conspecific brood parasitism by colonial red-breasted mergansers

Costs of conspecific brood parasitism (CBP) are expected to be influenced by a species’ life history traits. Precocial birds lay large clutches, and clutches that have been enlarged by CBP can affect host fitness through a longer incubation period, displaced eggs, and lower hatching success. We examined costs and response to CBP by hosts in a population of colonial red-breasted mergansers (Mergus serrator; n?=?400 nests over 8 years) within which 29% of parasitized clutches were enlarged considerably (≥?15 eggs). Length of the incubation period did not increase with clutch size. The mean number of eggs displaced from a parasitized nest during incubation (2.8) was 2×?greater than at an unparasitized nest (1.4). Hatching success declined by 2% for each additional egg in the nest. Thus, for a nest with?≥?15 eggs, one or more fewer host eggs hatch relative to an unparasitized nest with the same number of host eggs, assuming equal probability of success for all eggs. Hosts were 40% more likely to desert nests receiving 2 or 6 experimental eggs relative to unparasitized control nests, although it is unknown whether hens deserting a nest renested elsewhere. Our study indicates that costs of CBP to hosts during nesting may be limited to those red-breasted mergansers incubating the largest clutches (≥?15 eggs), and it raises questions about the adaptive significance of deserting a parasitized clutch.     

Are Cuckoos Maximizing Egg Mimicry by Selecting Host Individuals with Better Matching Egg Phenotypes?

Background

Avian brood parasites and their hosts are involved in complex offence-defense coevolutionary arms races. The most common pair of reciprocal adaptations in these systems is egg discrimination by hosts and egg mimicry by parasites. As mimicry improves, more advanced host adaptations evolve such as decreased intra- and increased interclutch variation in egg appearance to facilitate detection of parasitic eggs. As interclutch variation increases, parasites able to choose hosts matching best their own egg phenotype should be selected, but this requires that parasites know their own egg phenotype and select host nests correspondingly.

Methodology/Principal Findings

We compared egg mimicry of common cuckoo Cuculus canorus eggs in naturally parasitized marsh warbler Acrocephalus palustris nests and their nearest unparasitized conspecific neighbors having similar laying dates and nest-site characteristics. Modeling of avian vision and image analyses revealed no evidence that cuckoos parasitize nests where their eggs better match the host eggs. Cuckoo eggs were as good mimics, in terms of background and spot color, background luminance, spotting pattern and egg size, of host eggs in the nests actually exploited as those in the neighboring unparasitized nests.

Conclusions/Significance

We reviewed the evidence for brood parasites selecting better-matching host egg phenotypes from several relevant studies and argue that such selection probably cannot exist in host-parasite systems where host interclutch variation is continuous and overall low or moderate. To date there is also no evidence that parasites prefer certain egg phenotypes in systems where it should be most advantageous, i.e., when both hosts and parasites lay polymorphic eggs. Hence, the existence of an ability to select host nests to maximize mimicry by brood parasites appears unlikely, but this possibility should be further explored in cuckoo-host systems where the host has evolved discrete egg phenotypes.     

Intraspecific nest parasitism in the grey starling (Sturnus cineraceus)

We studied intraspecific nest parasitism in the grey starling (Sturnus cineraceus) in 1992 and 1993. We used three criteria to detect nest parasitism: (i) the appearance of more than one egg per day while the host was laying; (ii) the appearance of extra eggs after the host completed its clutch; and (iii) the appearance of eggs which were of a different shape, size and color to other eggs in the clutch. There were 290 nests (157 nests in 1992; 133 nests in 1993) in which the clutch was completed early (clutches initiated before May 10). Twenty-nine (1992) and 32 (1993) nests contained at least one parasitic egg. Parasitic eggs hatched if they were laid during the laying period and early in the incubation period of their host, and a few of them fledged. Fledging success of parasitic eggs was not different from that of eggs in non-parasitized nests if parasitic eggs were laid during the host's laying period. However, fledging success of all parasitic eggs was fewer than that of eggs in non-parasitized nests. By comparison, fledging success of parasitized nests was not a great as that of non-parasitized nests.     

The costs of avian brood parasitism explain variation in egg rejection behaviour in hosts

Many bird species can reject foreign eggs from their nests. This behaviour is thought to have evolved in response to brood parasites, birds that lay their eggs in the nest of other species. However, not all hosts of brood parasites evict parasitic eggs. In this study, we collate data from egg rejection experiments on 198 species, and perform comparative analyses to understand the conditions under which egg rejection evolves. We found evidence, we believe for the first time in a large-scale comparative analysis, that (i) non-current host species have rejection rates as high as current hosts, (ii) egg rejection is more likely to evolve when the parasite is relatively large compared with its host and (iii) egg rejection is more likely to evolve when the parasite chick evicts all the host eggs from the nest, such as in cuckoos. Our results suggest that the interactions between brood parasites and their hosts have driven the evolution of egg rejection and that variation in the costs inflicted by parasites is fundamental to explaining why only some host species evolve egg rejection.     

Cuckoo parasitism in a cavity nesting host: near absent egg‐rejection in a northern redstart population under heavy apparent (but low effective) brood parasitism

Brood parasite – host systems continue to offer insights into species coevolution. A notable system is the redstart Phoenicurus phoenicurus parasitized by the ‘redstart‐cuckoo’ Cuculus canorus gens. Redstarts are the only regular cuckoo hosts that breed in cavities, which challenges adult cuckoos in egg laying and cuckoo chicks in host eviction. We investigated parasitism in this system and found high overall parasitism rates (31.1% of 360 redstart nests), but also that only 33.1% of parasitism events (49 of 148 eggs) were successful in laying eggs into redstart nest cups. The majority of cuckoo eggs were mislaid and found on the rim of the nest; outside the nest cup. All available evidence suggests these eggs were not ejected by hosts. The effective parasitism rate was therefore only 12.8% of redstart nests. Redstarts responded to natural parasitism by deserting their nests in 13.0% of cases, compared to desertion rates of 2.8% for non‐parasitized nests. Our egg parasitism experiments found low rates (12.2%) of rejection of artificial non‐mimetic cuckoo eggs. Artificial mimetic and real cuckoo eggs added to nests were rejected at even lower rates, and were always rejected via desertion. Under natural conditions, only 21 cuckoo chicks fledged of 150 cuckoo eggs laid. Adding to this low success, is that cuckoo chicks are sometimes unable to evict all host young, and were more likely to die as a result compared to cuckoo chicks reared alone. This low success seems to be mainly due to the cavity nesting strategy of the redstart which is a challenging obstacle for the cuckoo. The redstart‐cuckoo system appears to be a fruitful model system and we suggest much more emphasis should be placed on frontline defences such as nest site selection strategies when investigating brood parasite–host coevolution.     

Common Cuckoos Cuculus canorus change their nest‐searching strategy according to the number of available host nests

In recent decades, numerous studies have examined factors affecting risk of host nest parasitism in well‐known avian host–parasite systems; however, little attention has been paid to the role of host nest availability. In accordance with other studies, we found that nest visibility, reed density and timing of breeding predicted brood parasitism of Great Reed Warblers Acrocephalus arundinaceus by the Common Cuckoo Cuculus canorus. More interestingly, hosts had a greater chance of escaping brood parasitism if nesting was synchronized. Cuckoo nest searching was governed primarily by nest visibility at high host‐nest density. However, even well‐concealed nests were likely to be parasitized during periods when just a few hosts were laying eggs, suggesting that Cuckoos adjust their nest‐searching strategy in relation to the availability of host nests. Our results demonstrate that host vulnerability to brood parasitism varies temporally and that Cuckoo females are able to optimize their nest‐searching strategy. Moreover, our study indicated that Cuckoos always manage to find at least some nests to parasitize. Thus, in this case, the co‐evolutionary arms race should take place mainly in the form of parasitic egg rejection rather than via frontline pre‐parasitism defence.     

Egg rejection in a passerine bird: size does matter

Avian brood parasites reduce the reproductive success of their hosts, selecting for the evolution of egg discrimination by the host, and potentially creating a coevolutionary arms race between host and parasite. Host egg discrimination ability is crucial in determining whether the arms race results in extinction (of the parasite on a particular host) or stable coevolutionary equilibrium of the host-parasite pair. I examined egg discrimination behaviour in the yellow-browed leaf warbler, Phylloscopus humei, a presumed former host of parasitic cuckoos, to show how discrimination ability has become very strong. Field experiments using model eggs demonstrate that rejection decisions are based on the relative size of eggs in the clutch. Individuals do not learn the particular size of their own eggs, but will accept both large and small eggs as long as all eggs in the clutch are of similar size. Host rejection decisions are continuously modified based on assessment of variation in egg sizes currently in the clutch, making it a difficult strategy for a cuckoo to defeat. Copyright 2000 The Association for the Study of Animal Behaviour.     

Cuckoos versus reed warblers: Adaptations and counteradaptations

At study sites in Cambridgeshire, England, the percentage of reed warbler, Acrocephalus scirpaceus, nests parasitized by cuckoos, Cuculus canorus, in 2 years was 22·5% and 9·1%. The warblers rejected cuckoo eggs at 19% of parasitized nests. Parasitized clutches suffered less predation than unparasitized clutches, suggesting that the cuckoo itself was the major predator, plundering nests too advanced for parasitism so that the hosts would re-lay. The cuckoos laid a mimetic egg, parasitized nests in the afternoons during the host laying period, usually removed one host egg, laid a remarkably small egg and laid very quickly. Nests were experimentally parasitized with model eggs to study the significance of this procedure. Experiments showed that host discrimination selects for: (1) egg mimicry by cuckoos (poorer matching model eggs were more likely to be rejected); (2) parasitism during the laying period (mimetic eggs put in nests before host laying began were rejected); (3) afternoon laying (mimetic eggs were less likely to be accepted in the early morning than in the afternoon, when hosts were more often absent from the nest); (4) a small egg (large eggs, typical of non-parasitic cuckoos, were more likely to be rejected); (5) rapid laying (a stuffed cuckoo on the nest stimulated increased rejection of model eggs), and (6) sets a limit to host egg removal by cuckoos (if more than one or two are removed desertion may occur). Mimicry may also be selected for because it reduced the chance that second cuckoos can discriminate the first cuckoo's egg from the host's clutch. Predation did not select for mimicry; nests with a non-mimetic egg did not suffer greater predation than those with a mimetic egg. Host rejection of model eggs did not depend on: (1) stage of parasitism once host egg laying had begun (nevertheless cuckoos were more likely to lay early in the host laying period probably to increase the chance the cuckoo chick hatched); (2) removal of a host egg (however, this reduced the incidence of unhatched eggs so cuckoos may remove a host egg so as not to exceed the host incubation limit). There were two costs of rejection, an ‘ejection’ cost (own eggs ejected as well as the cuckoo egg) and, with mimetic eggs, a ‘recognition’ cost (own eggs ejected instead of the cuckoo egg). Reed warblers did not discriminate against unlike chicks (another species) and did not favour either a cuckoo chick or their own chicks when these were placed in two nests side by side. Possible reasons why the hosts discriminate against unlike eggs but not unlike chicks are discussed.     

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.     

Egg ejection cost can limit defence strategies against brood parasitism

A cost associated with the evolution of antiparasite strategies is the failure to recognize parasitic eggs, leading the host to evict its own eggs. However, there is evidence that birds recognize their own eggs through imprinting. This leads to the question of why birds accept parasitic eggs if such eggs can be identified. Here, we tested whether egg ejection per se can be costly due to increased predation risk to the remaining clutch and whether olfactory or visual cues of egg ejection increase predation. We carried out three field experiments to answer the following questions: (a) Does ejecting an egg increase nest predation risk? (b) Does the presence of olfactory cues, such as the smell of a broken egg, increase nest predation risk? And (c) Does the presence of visual cues, such as an egg shell below the nest, increase nest predation risk? We found evidence that egg ejection increases nest predation and that olfactory cues alone also increase nest predation. The presence of visual cues did not change predation rates. These data indicate that egg ejection is costly for both host and parasitic eggs that may remain in the nest. Our results suggest why host and parasite eggs are commonly found within the same nests, despite the possibility that hosts recognize and could possibly eject the parasite’s egg.