The Perceptual and Cognitive Processes That Govern Egg Rejection in Hosts of Avian Brood Parasites

Hosts of avian brood parasites are under intense selective pressure to prevent or reduce the cost of parasitism. Many have evolved refined egg discrimination abilities, which can select for eggshell mimicry in their parasite. A classic assumption underlying these coevolutionary dynamics is that host egg recognition depends on the perceivable difference between their own eggs and those of their parasite. Over the past two decades, the receptor noise-limited (RNL) model has contributed to our understanding of these coevolutionary interactions by providing researchers a method to predict a host’s ability to discriminate a parasite’s egg from its own. Recent research has shown that some hosts are more likely to reject brown eggs than blue eggs, regardless of the perceived differences to their own. Such responses suggest that host egg recognition may be due to perceptual or cognitive processes not currently predictable by the RNL model. In this perspective, we discuss the potential value of using the RNL model as a null model to explore alternative perceptual processes and higher-order cognitive processes that could explain how and why some hosts make seemingly counter-intuitive decisions. Further, we outline experiments that should be fruitful for determining the perceptual and cognitive processing used by hosts for egg recognition tasks.

The Role of Intra-Clutch Variation of Magpie Clutches in Foreign Egg Rejection Depends on the Egg Trait Considered

The existence of a coevolutionary process between avian brood parasites and their hosts predicts a lower intra-clutch variation in egg appearance of host eggs among rejecters as this would favor egg discrimination of parasite eggs by hosts once parasitic egg mimicry had evolved. So far empirical tests of this prediction have ignored the fact that different aspects of host egg phenotypes may differ in the relative role of environmental vs. genetic determination, and hence that the role of intra-clutch variation in egg rejection within a population cannot be invariant. Here, we estimated whether the intra-clutch variation in several aspects of host eggshell features is consistently associated to rejection of parasitic foreign eggs across years in a magpie host population parasitized by great spotted cuckoos. We innovatively estimated spottiness by means of the fractal dimension of eggs, which considers the homogeneity of spot pattern complexity in eggshells. Our results show that low intra-clutch variation in the blue-green coloration at the middle area of the eggs associated with a high chance of rejection, but only in one of the 3 years we conducted the study. In addition, females that rejected foreign eggs presented more homogenous spot patterns in their clutches as estimated by their fractal dimension than females that accepted experimental eggs, independently of the year of study. Finally, intra-clutch variation in egg volume of host eggs was not associated to rejection. Analyses at the individual level revealed that the relative role of genetic vs. environmental factors that determine egg phenotype would be feature-specific in magpies, females having a characteristic spottiness, but not color or volume, pattern. Our work stresses the importance of considering a holistic approach including several aspects of variation in host egg phenotype (size, color, and homogeneity of spot pattern), as some aspects might be more susceptible to selection through egg rejection than others, presumably because they are less influenced by variation in the environmental conditions. Moreover, our study highlights the importance of replication in studies on the adaptive value of host traits in egg rejection.

Analysis of Egg Variation and Foreign Egg Rejection in Rüppell’s Weaver (Ploceus galbula)

Egg appearance is notable for its variation and as a source of recognition cues in bird species that are subject to egg-mimicking brood parasitism. Here I analyze the egg appearance of an East African weaverbird species that has variable eggs and is a host of brood parasitism by an egg-mimicking cuckoo, in order to (1) compare population variation to variation within a clutch as a measure of the distinctiveness of eggs; (2) assess modularity versus correlation among egg appearance traits as an indication of the complexity of egg signatures; and (3) address whether the eggs are discretely polymorphic or continuously variable in appearance. I also compare three methods of assessing egg coloration: reduction of spectral data to orthogonal components, targeted spectral shape variables, and avian visual modeling. Then I report the results of egg replacement experiments that assess the relationship between egg rejection behavior and the difference in appearance between own and foreign eggs. Rüppell’s weaver (Ploceus galbula) eggs are variable in appearance between individuals and consistent within a clutch, but vary widely in the distinctiveness of particular traits. Most aspects of color and spotting are decoupled from each other, including coloration likely to derive from different pigments. Egg ground color is bimodal, with a broad continuous class of off-white/UV eggs and another broad class of blue-green eggs. Variation in all other traits is unimodal and usually normal in distribution. Females reject foreign eggs on the basis of the difference in brightness of the ground color and spotting of foreign eggs relative to their own, and the difference in degree to which spots are aggregated at the broad end of the egg. This aggregation is among the most distinctive features of their eggs, but the brightness of the ground color and spotting brightness are not; the birds’ use of brightness rather than the more distinctive chromatic variation to recognize eggs might reflect the salience of achromatic contrast in a dim enclosed nest.

Egg rejection and egg recognition mechanisms in Oriental Reed Warblers

Background Nest parasitism by cuckoos (Cuculus spp.) results in enormous reproductive failure and forces hosts to evolve antiparasitic strategies, i.e., recognition of own eggs and rejection of cuckoo eggs. There are often sexual conflicts between male and female individuals in the expression of antiparasitic behavior due to the differences in reproductive inputs and division of labor. Methods By adding a foreign egg made of blue soft clay to the host nest during early incubation period in the field, and by removing several host eggs and adding experimental eggs to control the proportion of two egg types in the nest, we examined egg rejection ability, egg recognition mechanism and sexual difference in egg rejection of the Oriental Reed Warbler (Acrocephalus orientalis), one of the major hosts of Common Cuckoos (Cuculus canorus). Results Our results indicated that Oriental Reed Warblers can recognize and reject nearly 100% (73/75) of the non-mimetic eggs made of blue soft clay, and they could reject foreign eggs with 100% accuracy, regardless of the ratio of experimental eggs and its own eggs in the nest. Furthermore, all cases of egg rejections recorded by videos were only carried out by females. Conclusions Oriental Reed Warblers have a high egg recognition ability and show a true recognition mechanism. Only female warblers perform egg rejection, suggesting that the sex for host egg incubation seems to play an important role in the evolution of egg recognition mechanisms.

Testing the Interspecific Function of Female Common Cuckoo “Bubbling” Call

Female common cuckoo (Cuculus canorous) predator-like “bubbling” calls distract host parental attention and reduce the egg rejection rate. Such “bubbling” calls are also frequently used to attract males and deter territorial rivals in intraspecies contact, and these calls are an ancestral character in many cuckoo species. Although hosts have had sufficient time to become familiar with this call and evolve anti-parasitic strategies, why are the hosts fooled by this “bubbling” call? We propose two hypotheses. The first hypothesis proposes that call variation reduces the opportunity for host species to correctly assess cuckoo tricks. In contrast, the second hypothesis proposes that the cost of behavior may prevent the antiparasitic strategy from evolving. In the study, we tested the prerequisites of these hypotheses, by investigating whether cuckoo calls vary during the day and testing whether the predator-like calls suppress bird activities. Based on field recordings from three different areas, we found high overlap in the calls generated during different periods. Oriental great reed warblers (Acrocephalus orientalis), a host species, did not show different responses toward the playback of female common cuckoo calls generated before noon or afternoon. Based on bird count data, we found that predator-like call playback is insufficient for suppressing bird activities. Therefore, none of the prerequisites were supported by our field data. We discuss the potential reasons for our findings and hope to inspire more research examining female cuckoo vocalizations.

Coevolution between Himalayan cuckoos and two sympatric Pycnonotidae hosts

Selection due to cuckoo parasitism is responsible for the evolution of anti-parasitism defenses in hosts. Different host species breeding sympatrically with a single parasitic cuckoo may evolve different strategies to reduce the risk or counter cuckoo parasitism, resulting in different interactions between cuckoos and hosts in areas of sympatry. Here, we studied the coevolutionary interactions between Himalayan cuckoos Cuculus saturatus and two sympatric and closely related potential hosts belonging to the family Pycnonotidae, the brown-breasted bulbul Cuculus saturatus and the collared finchbill Spizixos semitorques. We investigated parasitism rates and nest site selection (nest height, nest cover, human disturbance, perch height, forest distance, and degree of concealment) related to parasitism risk, nest defense against a cuckoo dummy, and egg rejection against cuckoo model eggs. Bulbuls used specific nest sites that were further away from forests than those of finchbills, and they behaved more aggressively toward cuckoos than finchbills. In contrast, bulbuls possessed moderate egg rejection ability, while the finchbill rejected 100% of cuckoo model eggs. We suggest that selection of a nest site away from forests by the bulbul explains the absence of parasitism by Himalayan cuckoos. We suggest that these interspecific differences in nest site selection and nest defense indicate alternative responses to selection due to cuckoos.

A Meta-Analysis of Avian Egg Traits Cueing Egg-Rejection Defenses Against Brood Parasitism

The capability of hosts to reject the odd egg from their nest is one of the key defenses against avian brood parasitism. Considerable research effort has been devoted to exploring which phenotypic traits of eggshells facilitate to cue the recognition of the parasitic egg. Here we have reviewed studies addressing salient egg traits involved in the rejection of foreign eggs and used a formal meta-analysis to quantify their relative importance. Hosts appear to rely to a large extent on eggshell color traits, followed by maculation patterns. Hosts respond with similar rates of egg rejection to natural vs. model eggs and when breeding in both closed and open nests. Analyses of experiments on hosts of Cuculus and Molothrus parasites, the two best studied brood parasitic lineages with different co-evolutionary histories, yield similar conclusions. We also identify several poorly studied potential egg recognition cues, such as odor or weight, and recommend exploring even the visual traits in more detail, including chromatic and achromatic contrasts or experimentally manipulated egg maculation characteristics. Recent technological and sensory ecological advances open many new research avenues to experimentally examine the role of diverse egg characteristics in antiparasite defenses.

Impact of nest sanitation behavior on hosts’ egg rejection: An empirical study and meta-analyses

Egg rejection in birds is a specific adaptation toward avian brood parasitism, while nest sanitation is a general behavior for cleaning the nest and avoiding predation. However, both behaviors refer to the action of ejecting objects out of the nest, and nest sanitation has been proposed as a pre-adaptation for egg rejection. Here we tested the eliciting effect of nest sanitation on egg rejection in the red-whiskered bulbul Pycnonotus jocosus, a potential host species that is sympatric with parasitic cuckoos. We conducted meta-analyses of previous studies on both nest sanitation and egg rejection, in order to evaluate the consistency of our conclusions. Our results showed that nest sanitation did not elicit egg rejection in P. jocosus. The conclusions concerning such an eliciting effect from previous studies were mixed, while the methodologies were inconsistent, making the studies unsuitable for comparisons. However, the ejection frequency of nest sanitation was consistently higher than the frequency of egg rejection across different host species or populations. These results suggest that nest sanitation, which is an ancient behavior, is more fundamental than egg rejection, but the effect of the former on the latter is complex and needs further study. Standardized methodologies and the integration of behavior, physiology, and modeling may provide better opportunities to explore the relationship between nest sanitation and egg rejection.

Host personality predicts cuckoo egg rejection in Daurian redstarts Phoenicurus auroreus

In species that are subject to brood parasitism, individuals often vary in their responses to parasitic eggs, with some rejecting the eggs while others do not. While some factors, such as host age (breeding experience), the degree of egg matching and the level of perceived risk of brood parasitism have been shown to influence host decisions, much of the variation remains unexplained. The host personality hypothesis suggests that personality traits of the host influence its response to parasitic eggs, but few studies have tested this. We investigated the relationship between two personality traits (exploration and neophobia) and a physiological trait (breathing rate) of the host, and egg-rejection behaviour in a population of Daurian redstarts Phoenicurus auroreus in northeast China. We first show that exploratory behaviour and the response to a novel object are repeatable for individual females and strongly covary, indicating distinct personality types. We then show that fast-exploring and less neophobic hosts were more likely to reject parasitic eggs than slow-exploring and more neophobic hosts. Variation in breathing rate—a measure of the stress-response—did not affect rejection behaviour. Our results demonstrate that host personality, along the bold-shy continuum, predicts the responses to parasitic eggs in Daurian redstarts, with bold hosts being more likely to reject parasitic eggs.