Foreign Eggs Research Articles

Breeding stages affect egg recognition in azure-winged magpies (Cyanopica cyanus)

Egg rejection often involves a cognitive process of recognizing foreign eggs, which can vary not only between species or among different individuals of the same species, but also within the same individual during different breeding stages, leading to markedly different responses to parasitic eggs. We conducted a comparative study in Wuhan, Hubei, and Fusong, Jilin, China, on the recognition and rejection behavior of azure-winged magpies (Cyanopica cyanus) at different breeding stages (pre-egg-laying, one-host-egg, multi-host-egg and early incubation stages). In the Fusong population, there was a significant difference in the rejection rate of model eggs by azure-winged magpies at different stages of the egg-laying period. During the one-host-egg stage, the rejection rate (63.6%) was significantly lower than that during the pre-egg-laying stage (85.7%) and the multi-host-egg stage (100%). The population of azure-winged magpies in Wuhan exhibited a 100% rejection rate towards model eggs during the pre-egg-laying stage. Furthermore, during the incubation stage, azure-winged magpies were able to accurately recognize and reject foreign eggs even when those were in majority. This indicates that azure-winged magpies employ a template-based recognition mechanism rather than relying on discordance mechanism for recognition after the onset of incubation. This study suggests that while azure-winged magpies can truly recognize their own eggs, different breeding stages still influence their rejection response towards parasitic eggs, especially during the pre-egg-laying and egg laying stages.

Common cuckoo eggs are more resistant to puncture by the host

The puncture resistance hypothesis suggests that thick-shelled eggs of parasitic birds can resist puncture-ejection by the host. However, few experiments have yet been conducted to test this hypothesis in terms of natural host behavior (e.g., pecking at foreign eggs). To explore whether the eggshells of common cuckoos (Cuculus canorus) are resistant to puncture-ejection by their common hosts, Oriental reed warblers (Acrocephalus orientalis), we designed experiments to investigate if and how breeding Oriental reed warblers peck at foreign eggs that includes common cuckoo, Oriental reed warbler and budgerigar (Melopsittacus undulatus) eggs. The results showed that, given the same frequency of egg pecking, the probability of eggshell breakage was 87.5% for eggs of the Oriental reed warbler and 0% for eggs of the common cuckoo, with a significant difference (P = 0.001, Fisher's exact test). Our study shows clearly that common cuckoos' eggshells are less susceptible to puncture-ejection than those of Oriental reed warblers and budgerigars. This indicates that the eggshells of common cuckoos can resist host Oriental reed warblers' puncture-ejection, supporting the puncture resistance hypothesis.

Innate and learned components of egg recognition in the ant Camponotus floridanus.

Insect societies discriminate against foreigners to avoid exploitation. In ants, helper workers only accept individuals with the familiar chemical cues of their colony. Similarly, unfamiliar eggs may get rejected at their first appearance in the nest. We investigated egg acceptance mechanisms by introducing different types of foreign eggs into worker groups of the ant Camponotus floridanus. Workers from established colonies familiar with queen-laid eggs always accepted eggs from highly fecund queens, but worker-laid eggs only after exposure for several weeks. Workers naive to eggs only rejected worker-laid eggs once they had prior exposure to eggs laid by highly fecund queens, suggesting that prior exposure to such eggs is necessary for discrimination. The general acceptance of eggs from highly fecund queens, irrespective of previous worker egg exposure, suggests an innate response to the queen pheromone these eggs carry. Workers learned to accept queen-laid eggs from different species, indicating high flexibility in learning egg-recognition cues. In incipient colonies with queen-laid eggs that carry a weak queen pheromone, worker-laid eggs were more likely to get accepted than queen-laid eggs from a different species, suggesting that the similarity of egg-recognition cues between the two types of C. floridanus eggs increases acceptance.

Recognition and rejection of foreign eggs of different colors in Barn Swallows

Brood parasitic birds lay eggs in the nests of other birds, and the parasitized hosts can reduce the cost of raising unrelated offspring through the recognition of parasitic eggs. Hosts can adopt vision-based cognitive mechanisms to recognize foreign eggs by comparing the colors of foreign and host eggs. However, there is currently no uniform conclusion as to whether this comparison involves the single or multiple threshold decision rules. In this study, we tested both hypotheses by adding model eggs of different colors to the nests of Barn Swallows (Hirundo rustica) of two geographical populations breeding in Hainan and Heilongjiang Provinces in China. Results showed that Barn Swallows rejected more white model eggs (moderate mimetic to their own eggs) and blue model eggs (highly non-mimetic eggs with shorter reflectance spectrum) than red model eggs (highly non-mimetic eggs with longer reflectance spectrum). There was no difference in the rejection rate of model eggs between the two populations of Barn Swallows, and clutch size was not a factor affecting egg recognition. Our results are consistent with the single rejection threshold model. This study provides strong experimental evidence that the color of model eggs can has an important effect on egg recognition in Barn Swallows, opening up new avenues to uncover the evolution of cuckoo egg mimicry and explore the cognitive mechanisms underlying the visual recognition of foreign eggs by hosts.

Host learning selects for the coevolution of greater egg mimicry and narrower antiparasitic egg-rejection thresholds.

Egg rejection is an effective and widespread antiparasitic defense to eliminate foreign eggs from the nests of hosts of brood parasitic birds. Several lines of observational and critical experimental evidence support a role for learning by hosts in the recognition of parasitic versus own eggs; specifically, individual hosts that have had prior or current experience with brood parasitism are more likely to reject foreign eggs. Here we confirm experimentally the role of prior experience in altering subsequent egg-rejection decisions in the American robin Turdus migratorius, a free-living host species of an obligate brood parasite, the brown-headed cowbird Molothrus ater. We then model the coevolutionary trajectory of both the extent of mimicry of host eggs by parasitic eggs and the host's egg rejection thresholds in response to an increasing role of learning in egg recognition. Critically, with more learning, we see the evolution of both narrower (more discriminating) rejection thresholds in hosts and greater egg mimicry in parasites. Increasing host clutch size (number of eggs/nest) and increasing parasite load (parasitism rate) also have narrowing effects on the egg-rejection threshold. Together, these results suggest that learning from prior experience with egg rejection may play an important role in the coevolution of egg-mimetic lineages of brood parasites and the refined egg rejection defenses of hosts.

When perfection isn't enough: host egg signatures are an effective defence against high-fidelity African cuckoo mimicry.

Most mimicry systems involve imperfect mimicry, whereas perfect and high-fidelity mimicry are rare. When the fidelity of mimicry is high, mimics might be expected to have the upper hand against their antagonists. However, in coevolving systems, diversification of model phenotypes may provide an evolutionary escape, because mimics cannot simultaneously match all model individuals in the population. Here we investigate high-fidelity mimicry in a highly specialized, Afrotropical brood parasite-host system: the African cuckoo and fork-tailed drongo. Specifically, we test whether host egg polymorphisms are an effective defence against such mimicry. We show, using a combination of image analysis, field experiments and simulations, that: (1) egg colour and pattern mimicry of fork-tailed drongo eggs by African cuckoos is near-perfect on average; (2) drongos show fine-tuned rejection of foreign eggs, exploiting unpredictable pattern differences between parasitic eggs and their own; and (3) the high degree of interclutch variation (polymorphic egg 'signatures') exhibited by drongos gives them the upper hand in the arms race, with 93.7% of cuckoo eggs predicted to be rejected, despite cuckoos mimicking the full range of drongo egg phenotypes. These results demonstrate that model diversification is a highly effective defence against mimics, even when mimicry is highly accurate.

Decision rules for egg-color-based rejection by two cavity-nesting hosts of the brown-headed cowbird.

Hosts of obligate avian brood parasites often evolve defense mechanisms to avoid rearing unrelated young. One common defense is egg rejection, for which hosts often rely on eggshell color. Most research has assumed that hosts respond to perceived color differences between their own eggs and parasite eggs regardless of the particular color; however, recent experiments have found that many hosts respond more strongly to brown foreign eggs than to equally dissimilar blue eggs. Yet, none of these prior studies tested a brown-egg-laying species and, with only one exception, all were conducted in open nests where light levels are considered sufficient for effective color-based egg discrimination. Here, we explored how two cavity-nesting hosts of the parasitic brown-headed cowbird (Molothrus ater) - the blue-egg-laying eastern bluebird (Sialia sialis) and the brown-egg-laying house wren (Troglodytes aedon) - respond to experimental eggs painted six distinct colors ranging from blue to brown. Rejection responses of both hosts were best predicted by perceived differences in color between the model egg and their own eggs. Specifically, we found that house wrens preferentially rejected eggs bluer than their own eggs. However, although we found that bluebirds relied on perceived differences in color for their egg rejection decisions, further tests are needed to determine whether they preferentially rejected brown eggs or simply responded to absolute perceived differences in color. These findings demonstrate that these cavity-nesting birds treat perceived color differences in distinct ways, which has important implications on the coevolutionary arms races and the interpretation of avian-perceived color differences.

Examining causes and characteristics of egg ejection behaviour in the American robin (Turdus migratorius)

Abstract American robins (Turdus migratorius) are among few hosts of parasitic brown-headed cowbirds (Molothrus ater) that frequently eject foreign eggs from their nests. However, we know little about some characteristics of the robins’ egg ejection process including its distance and direction. We used a novel technique (i.e., radio transmitters inserted into 3D-printed eggshells) to examine egg rejection in female robins as a function of model egg coloration (i.e., robin-mimetic blue, non-mimetic deep blue, and non-mimetic beige). Based on prior work, we predicted that female robins’ egg ejection decisions would be dependent on egg coloration. Accordingly, we found a significant effect of female identity (using nest identity as a proxy) and model egg colour on egg ejection, but neither predicted ejection distance or direction. Deep blue model eggs had shorter ejection latencies than beige eggs. Fully characterizing the egg ejection process will allow us to further understand the mechanisms and outcomes of egg ejection behaviours in host-parasite interactions.

Multiple parasitism promotes facultative host acceptance of cuckoo eggs and rejection of cuckoo chicks

Many hosts of brood-parasitic cuckoos reject foreign eggs from the nest. Yet where nests commonly receive more than one cuckoo egg, hosts might benefit by instead accepting parasite eggs. This is because cuckoos remove an egg from the nest before adding their own, and keeping cuckoo eggs in the nest reduces the odds that further host eggs are removed by subsequent cuckoos. This ‘clutch dilution effect’ has been proposed as a precondition for the evolution of cuckoo nestling eviction by hosts, but no previous studies have tested this in a host that rejects cuckoo nestlings. We tested the clutch dilution hypothesis in large-billed gerygones, Gerygone magnirostris, which are multiply parasitized by little bronze-cuckoos, Chalcites minutillus. Gerygones evict cuckoo nestlings but accept cuckoo eggs. Consistent with multiple parasitism favouring egg acceptance, we found gerygone egg survival was higher under scenarios of cuckoo egg acceptance than rejection. Yet gerygones were also flexible in their egg acceptance, with 61% abandoning clutches if they contained only cuckoo eggs. Our results thus confirm a clutch dilution effect in gerygones and suggest that multiple parasitism might favour a facultative response to cuckoo eggs, whereby hosts accept or reject cuckoo eggs depending on clutch composition.

Patterns of stress response to foreign eggs by a rejecter host of an obligate avian brood parasite.

One of the most effective defenses of avian hosts against obligate brood parasites is the ejection of parasitic eggs from the nests. Despite the clear fitness benefits of this behavior, individuals within so-called "egg-rejecter" host species still show substantial variation in their propensity to eliminate foreign eggs from the nest. We argue that this variation can be further understood by studying the physiological mechanisms of host responses to brood parasitic egg stimuli: independent lines of research increasingly support the hypothesis that stress-related physiological response to parasitic eggs may trigger egg rejection. The "stress-mediated egg rejection" hypothesis requires that hosts activate the stress-response when responding to parasitic egg stimuli. We tested this prediction by asking whether hosts showed differential stress response when exposed to host-like (mimetic) or parasite-like (non-mimetic) eggs. We experimentally parasitized incubating American robins Turdus migratorius, a robust egg-rejecter host to obligate brood parasitic brown-headed cowbirds Molothrus ater, with mimetic or non-mimetic model eggs. To assess the stress response, we measured the heart rate in incubating females immediately after experimental parasitism. We also measured plasma corticosterone and, in a subset of birds, used RNA-sequencing to analyze the expression of proopiomelanocortin (POMC), a precursor of adrenocorticotropic hormone, 2 h after experimental parasitism. We found that egg type had no effect on heart rate. Two hours following experimental parasitism, plasma corticosterone did not differ between the differently-colored model egg treatments or between rejecter and accepter females within the non-mimetic treatment. However, females exposed to non-mimetic eggs showed an upregulation of POMC gene expression (before FDR correction) in the pituitary compared with females treated with mimetic eggs. Our findings suggest that in an egg-rejecter host species, non-mimetic parasitic eggs may increase the activity of the stress-related hypothalamic-pituitary-adrenal axis compared with mimetic eggs, although the temporaldynamics of this response are not yet understood.

Egg rejection and egg recognition mechanism in a Chinese Azure-winged Magpie (Cyanopica cyanus) population

Recognition and rejection of foreign eggs are effective defense of hosts against brood parasitism. However, brood parasitism can impose various selection pressures on different geographic populations of the same host species. In a multiple cuckoo system in China, Azure-winged Magpies (Cyanopica cyanus) are parasitized by both Indian Cuckoos (Cuculus micropterus) and Asian Koels (Eudynamys scolopaceus). In this study, egg recognition ability and recognition mechanism of the Azure-winged Magpie were investigated using a population in Fusong, southeastern Jilin, China. The results showed that 55.6% (20/36) of the Azure-winged Magpies correctly rejected quail (Coturnix japonica) eggs in their nests, while 13.9% (5/36) of the individuals experienced rejection costs by wrongly rejecting their own eggs. Azure-winged Magpies could accurately reject the experimental eggs when the number of such eggs in the nests was the same as that of the magpie eggs. However, Azure-winged Magpies do not recognize and reject conspecific eggs (0/28). The present study indicates that the Azure-winged Magpie has moderate egg recognition ability toward non-mimetic quail eggs and shows a true recognition mechanism with rejecting foreign eggs by accurately recognizing their own eggs. However, they cannot recognize conspecific eggs.

Non-invasive elevation of circulating corticosterone increases the rejection of foreign eggs in female American robins (Turdus migratorius)

Avian obligate brood parasites rely on other species to raise their offspring. In turn, many brood parasite hosts have evolved defensive behaviors to reduce the costs of brood parasitism, yet the proximate bases underlying these defenses remain poorly understood. Recent studies regarding the potential endocrine mechanisms of foreign-egg rejection have implicated corticosterone as a physiological mediator of anti-parasitic defenses. For example, corticosterone is elevated in response to non-mimetic eggs in an egg rejecter thrush, the Eurasian blackbird (Turdus merula) and this hormone's suppression reduces egg rejection rates in the congeneric American robin (T. migratorius). American robins are also among the few host species of obligate brood parasitic brown-headed cowbirds (Molothrus ater) that readily reject foreign eggs from their nests. We non-invasively elevated corticosterone levels in incubating female robins by dissolving it in DMSO gel which was then applied onto eggs already in the clutch. Relative to controls treated with pure DMSO gel, corticosterone-treated female robins were more likely to reject a non-mimetic, cowbird-sized foreign egg (72 %) than control females (50 %) when accounting for the known effect of lower clutch sizes on greater egg rejection. Future studies are needed to assess the sensory and cognitive impact(s) of corticosterone, as well as other hormones essential for parental care, in this and other hosts' defense behaviors against avian brood parasitism.

Egg Rejection: Getting Rid of a Parasite in the Nest

Some species of birds, called brood parasites, lay their eggs in the nests of other species (called the hosts). Male and female hosts take care of the parasitic offspring. In most cases, the hosts raise only the parasitic chicks, which reduces the breeding success of the host birds. However, hosts can defend themselves from brood parasitism by developing the ability to recognize and reject parasitic eggs from their nests. In this article, we explore how host age influences the ability to reject foreign eggs. We show that female magpies improve their ability to reject foreign eggs added to their nests as they age, and we discuss what this might mean for both the magpies and cuckoos. Our results might ultimately help us to better understand how animals and humans defend themselves against the disease-causing parasites that infect them.

Correlated evolution of eggshell maculation with social breeding and nest type in Hirundinidae

Maculation on avian eggshells has the potential to serve as an identity signal, and this information may help females recognize their eggs/nest or reject foreign eggs laid by hetero‐ or conspecific brood parasites. Recognizing eggs could be adaptive in cases where birds nest in dense colonies, as reports of conspecific brood parasitism are over‐represented in colony‐nesting species. We utilized the variation in breeding biology (solitary vs. colonial breeding) and eggshell phenotype in swallows and martins (Hirundinidae) to test for correlated evolution between these traits, while also accounting for nest type, as maculation may camouflage eggs in open‐cup nests. We found that maculated eggs were more likely to be laid by species that breed socially and build open‐cup nests where maculation would be more visible than in dark cavity nests.

Social transmission of egg rejection in a cuckoo host

Social learning can enable the rapid dissemination of behaviours throughout a population. Rejection of foreign eggs is a key defence used by hosts of avian brood parasites, and although learning has long been recognized as an important factor in egg rejection decisions, the role played by social cues remain less well understood. Here, we aimed to determine whether access to social information influenced egg rejection behaviours in semicolonial barn swallows, Hirundo rustica . By manipulating the social information available from a neighbouring nest, we showed that swallows with access to social information (i.e. a neighbour that recently rejected an egg) were more likely to reject a foreign egg that those that did not have access to social information (i.e. a neighbour that did not reject an egg). A subset of nests were videorecorded, and in these recordings the rejections were always performed by the incubating parent rather than a conspecific. This study provides direct evidence that egg rejection behaviours can be informed by social information in the absence of brood parasites, and in doing so highlights the dynamic nature of the defences that hosts deploy against brood parasitism. • Information about parasitism risk can inform host defences. • We tested whether social information could inform egg rejection decisions. • Barn swallows with access to social information rejected more foreign eggs. • Our results highlight the role that social information can play in coevolution.

Egg burial in the ringneck dove (Streptopelia risoria): A potential laboratory model system for egg-rejection research?

In avian brood parasitism, parasites lay their eggs in the nests of hosts, and many hosts in the wild respond by eliminating or abandoning foreign eggs in their clutch. However, a limitation upon the study of proximate, especially physiological and experience-dependent cognitive mechanisms of egg rejection, has been the lack of a suitable model system in captivity. Here, we tested whether laboratory-kept ringneck doves (Streptopelia risoria) respond to visually distinct egg types (through applying an ink treatment upon the doves' own eggs) by rejecting them. We found that in two of two experiments, brown eggs were more often rejected, through predominantly egg burial, relative to control eggs but were done so only by a subset of dove pairs. These results are supportive of ringneck doves to become a suitable captive model for the study of foreign-egg rejection, and open the way for future research on the integrative (e.g., genetic, endocrine, ontogenetic, and cognitive) study of egg-rejection responses in a tractable research system. However, the ecological validity and applicability of this model system for the analysis of host-parasite interactions in the wild remain narrowly limited. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Nest sanitation as an effective defence against brood parasitism.

Egg rejection is a crucial defence strategy against brood parasitism that requires the host to correctly recognise the foreign egg. Rejection behaviour has, thus, evolved in many hosts, facilitated by the visual differences between the parasitic and host eggs, and driving hosts to rely on colour and pattern cues. On the other hand, the need to recognise non-egg-shaped objects to carry out nest sanitation led birds to evolve the ability to discriminate and eject objects using mainly shape cues. However, little is known regarding the evolutionary significance of rejection behaviour in general and the cognitive processes underlying it. Here, we investigated the response of the barn swallow (Hirundo rustica) during pre-laying and laying stages to four objects types that differed in shape (eggs vs stars) and colour/pattern (mimetic vs non-mimetic) to investigate (1) what cognitive mechanisms are involved in object discrimination and (2) whether egg rejection is a direct defence against brood parasitism, or simply a product of nest sanitation. We found that swallows ejected stars more often than eggs in both stages, indicating that swallows possess a template for the shape of their eggs. Since the effect of colour/pattern on ejection decisions was minor, we suggest that barn swallows have not evolved a direct defence against brood parasitism but instead, egg ejection might be a product of their well-developed nest sanitation behaviour. Nonetheless, the fact that mimetic eggs were ejected especially in the pre-laying stage shows that nest sanitation could be an effective defence against poorly timed brood parasitism.

A review of the cues used for rejecting foreign eggs from the nest by the Eurasian blackbird (Turdus merula).

Avian brood parasitism is reproductively costly for hosts and selects for cognitive features enabling anti‐parasitic resistance at multiple stages of the host's breeding cycle. The true thrushes (genus Turdus) represent a nearly worldwide clade of potential hosts of brood parasitism by Cuculus cuckoos in Eurasia and Africa and Molothrus cowbirds in the Americas. The Eurasian blackbird (Turdus merula) builds an open‐cup nest and is common within much of the common cuckoo's (C. canorus) breeding range. While this thrush is known to be parasitized at most only at low rates by this cuckoo, the species is also a strong rejector of nonmimetic foreign eggs in the nest. Given their open‐cup nesting habits, we predict that Eurasian blackbirds primarily use visual cues in making a distinction between own and parasitically or experimentally inserted foreign eggs in the nest. We then provide a comprehensive and quantitative review of the literature on blackbird egg rejection studies. This review corroborates that vision is the primary sensory modality used by blackbirds in assessing eggs, but also brings attention to some other, less commonly studied cues which appear to influence rejection, including predator exposure, individual experience, stage of clutch completion, and maternal hormonal state. Blackbirds are also able to recognize and eject even highly mimetic eggs (including those of conspecifics) at a moderate rate, apparently relying on many of the same sensory cues. Although the cues involved in foreign egg recognition by Eurasian blackbirds do not appear specialized to nonmimetic cuckoo parasitism, we cannot differentiate between the possibility of egg rejection being selected by mostly conspecific parasitism or by the evolutionary ghost of a now‐extinct, mimetic cuckoo host‐race.

Thicker eggshells are not predicted by host egg ejection behaviour in four species of Australian cuckoo

Defences of hosts against brood parasitic cuckoos include detection and ejection of cuckoo eggs from the nest. Ejection behaviour often involves puncturing the cuckoo egg, which is predicted to drive the evolution of thicker eggshells in cuckoos that parasitise such hosts. Here we test this prediction in four Australian cuckoo species and their hosts, using Hall-effect magnetic-inference to directly estimate eggshell thickness in parasitised clutches. In Australia, hosts that build cup-shaped nests are generally adept at ejecting cuckoo eggs, whereas hosts that build dome-shaped nests mostly accept foreign eggs. We analysed two datasets: a small sample of hosts with known egg ejection rates and a broader sample of hosts where egg ejection behaviour was inferred based on nest type (dome or cup). Contrary to predictions, cuckoos that exploit dome-nesting hosts (acceptor hosts) had significantly thicker eggshells relative to their hosts than cuckoos that exploit cup-nesting hosts (ejector hosts). No difference in eggshell thicknesses was observed in the smaller sample of hosts with known egg ejection rates, probably due to lack of power. Overall cuckoo eggshell thickness did not deviate from the expected avian relationship between eggshell thickness and egg length estimated from 74 bird species. Our results do not support the hypothesis that thicker eggshells have evolved in response to host ejection behaviour in Australian cuckoos, but are consistent with the hypothesis that thicker eggshells have evolved to reduce the risk of breakage when eggs are dropped into dome nests.

Eggshell texture but not odor treatment affects model egg rejection in American robins (Turdus migratorius).

To curb fitness costs associated with obligate avian brood parasitism, some hosts have evolved to reject foreign eggs in the nest. American robins (Turdus migratorius) are among the few hosts of the brown-headed cowbird (Molothrus ater) that mostly remove parasitic eggs from their nests. With the parasite's eggs looking nothing like their own, American robins likely rely most on visual cues when making rejection decisions. However, we still know little about the roles thattactile and olfactory cues play in robin's or other rejecter hosts' rejection decisions. Here, we conducted a set of experiments to test for the use of tactile or olfactory cues in egg rejection by robins. For the tactile experiment, we found that robins were more likely to reject rough rather than smooth eggs. However, our tactile model egg design was not able to fully discriminate between tactile and visual sensorymodalities. In the olfaction experiment, we did not find a significant effect of egg scent treatment on rejection rates. Accordingly, future studies on egg rejection should attempt to fully distinguish between tactile and visual cues, as well as examine olfactory cues in other egg rejecter host species.