Egg discrimination in the Australian reed warbler (Acrocephalus australis): rejection response toward model and conspecific eggs depending on timing and mode of artificial parasitism

In a coevolutionary arms race between an interspecific broodparasite and its host species, both are expected to evolveadaptations and counteradaptations. We studied egg discriminationin the Australian warbler (Acrocephalus australis). This speciesis currently not significantly parasitized by the seven speciesof cuckoo for which it is a suitable host. However, experimentalbrood parasitism in the warbler revealed a fine tuned egg discriminationresponse towards non-mimetic and conspecific eggs, the firstsuch evidence in an Australian passerine: (1) non-mimetic eggswere significantly more often rejected than conspecific eggs;(2) only non-mimetic dummy eggs were rejected selectively,whereas rejection of conspecific eggs entailed a rejectioncost; (3) replacement of a host's egg with a conspecific eggduring egg laying resulted in a significantly higher rejectionrate than after the day of clutch completion; (4) by contrast,rejection rate after addition of a conspecific egg was independentof nest stage; (5) conspecific eggs introduced into a clutchduring the egg laying period led to a significantly highernest desertion rate and a lower egg ejection rate than afterthe day of clutch completion; and (6) addition of a conspecificegg led to egg ejection while egg replacement with a conspecificegg led to nest desertion. The fact that this species respondsdifferentially toward different modes of artificial parasitismsuggests that its egg discrimination has evolved to minimizethe costs of rejection and parasitism. The ability to rejecthighly mimetic conspecific eggs may explain the current paucityof brood parasitism in this species. The significance of thisfor brood parasite-host coevolution is discussed.     

The evolution of egg size in the brood parasitic cuckoos

We compared genera of nonparasitic cuckoos and two groups ofparasitic cuckoos: those raised together with host young ("nonejectors")and those in which the newly hatched cuckoo either ejects thehost eggs or chicks, or kills the host young ("ejectors"). Nonejectorsare similar to their hosts in body size and parasitize largerhosts than do ejectors, which parasitize hosts much smallerthan themselves. In both types of parasite, the cuckoo's eggtends to match the host eggs in size. To achieve this, nonejectorshave evolved a smaller egg for their body size than have nonparasiticcuckoos, and ejectors have evolved an even smaller egg. Amongejector cuckoo genera, larger cuckoos have larger eggs relativeto the eggs of their hosts, and the relationship between cuckooegg volume (mass of the newly-hatched cuckoo) and host egg volume(mass to be ejected) did not differ from that predicted by weight-liftingallometry. However, comparing among Cuculus cuckoo species,the allometric slope differed from the predicted, so it is notclear that egg size is related to the need to give the cuckoochick sufficient strength for ejection. Comparing the two mostspeciose ejector genera, Chrysococcyx cuckoos (smaller and parasitizedome-nesting hosts) lay eggs more similar in size to their host'seggs than do Cuculus cuckoos (larger and parasitize open cup–nestinghosts). Closer size-matching of host eggs in Chrysococcyx mayreflect the following: (1) selection to reduce adult body massto facilitate entry through small domed nest holes to lay, and(2) less need for a large egg, because longer incubation periodsin dome-nesting hosts allow the young cuckoo more time to growbefore it need eject host eggs.     

Nest sanitation behavior does not increase the likelihood of parasitic egg rejection in herring gulls

Birds’ behavioral response to brood parasitism can be influenced not only by evolution but also by context and individual experience. This could include nest sanitation, in which birds remove debris from their nests. Ultimately, nest sanitation behavior might be an evolutionary precursor to the rejection of parasitic eggs. Proximately, the context or experience of performing nest sanitation behavior might increase the detection or prime the removal of parasitic eggs, but evidence to date is limited. We tested incubation-stage nests of herring gulls Larus argentatus to ask whether nest sanitation increased parasitic egg rejection. In an initial set of 160 single-object experiments, small, red, blocky objects were usually rejected (18 of 20 nests), whereas life-sized, 3D-printed herring gull eggs were not rejected whether red (0 of 20) or the olive-tan base color of herring gull eggs (0 of 20). Next, we simultaneously presented a red, 3D-printed gull egg and a small, red block. These nests exhibited frequent nest sanitation (small, red block removed at 40 of 48 nests), but egg rejection remained uncommon (5 of those 40) and not significantly different from control nests (5 of 49) which received the parasitic egg but not the priming object. Thus, performance of nest sanitation did not shape individuals’ responses to parasitism. Interestingly, parents were more likely to reject the parasitic egg when they were present as we approached the nest to add the experimental objects. Depending on the underlying mechanism, this could also be a case of experience creating variation in responses to parasitism.     

Recognizing odd smells and ejection of brood parasitic eggs. An experimental test in magpies of a novel defensive trait against brood parasitism

One of the most important defensive host traits against brood parasitism is the detection and ejection of parasitic eggs from their nests. Here, we explore the possible role of olfaction in this defensive behaviour. We performed egg‐recognition tests in magpie Pica pica nests with model eggs resembling those of parasitic great spotted cuckoos Clamator glandarius. In one of the experiment, experimental model eggs were exposed to strong or moderate smell of tobacco smoke, whereas those of a third group (control) were cleaned with disinfecting wipes and kept in boxes containing odourless cotton. Results showed that model eggs with strong tobacco scent were more frequently ejected compared with control ones. In another experiment, models were smeared with scents from cloacal wash from magpies (control), cloacal wash or uropygial secretions from cuckoos, or human scents. This experiment resulted in a statistically significant effect of treatment in unparasitized magpie nests in which control model eggs handled by humans were more often rejected. These results provide the first evidence that hosts of brood parasites use their olfactory ability to detect and eject foreign eggs from their nests. These findings may have important consequences for handling procedures of experimental eggs used in egg‐recognition tests, in addition to our understanding of interactions between brood parasites and their hosts.     

Distribution and breeding ecology of the Ferruginous Duck Aythya nyroca in Algeria

We conducted a survey of the distribution of Ferruginous Duck Aythya nyroca across Algeria and analysed the influence of nest-site characteristics on nesting success at a Ramsar site, Lake Tonga. The species was found to occupy different wetlands (freshwater lakes, brackish marshes and salt lakes) across three major climatic belts (subhumid coastal strip, semi-arid Hauts Plateaux and arid Sahara). Mean clutch size of successful nests was 13.3 ± 6.0 eggs (N = 26) with a hatching rate of 74% for successful clutches. Nesting success was recorded for 44% of nests with clutch desertion (72.7%) accounting for the majority of failed clutches. Egg size of the study population, which breeds at the southern limit of the species’ range, was significantly smaller than that of its northerly counterparts. Clutch size was negatively related to egg size and positively associated with depth of water below the nest, suggesting that older, more experienced or high-quality birds monopolised the safest sites. Successful clutches were significantly associated with tall vegetation, suggesting that when nesting is carried out mainly on offshore floating islets, protection against aerial predators and heat stress determine nesting outcome. Conspecific brood parasitism was significantly and positively associated with deferred egg-laying and smaller egg size, suggesting an age-dependent mechanism.     

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

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

A comparative analysis of the evolution of variation in appearance of eggs of European passerines in relation to brood parasitism

Host of brood parasites increase the ability of rejecting cuckooeggs by production of (1) a clutch with little variation amongeggs and (2) a clutch that differs the most from the modal phenotypeof the population. These hypotheses have been tested by Øienet at. (1995), although they did not control for common phylogeneticancestry. We analyze the evolution of egg color and markingpatterns in European passerines, which are potential hosts ofdie European cuckoo (Cuculus canorus), using Felsenstein's (1985)independent comparative method to control for the effect ofcommon phylogenetic descent We found a significant positiverelationship between interclutch variation in appearance ofhost eggs and parasitism rate, but this relationship disappearedwhen hole-nesting species were excluded from the analysis; andwe found a highly significant multiple regression between rejectionrate and intra- and interclutch variation in egg appearance,even when hole nesters were excluded from the analysis. Thepartial correlation coefficients were negative for intraclutchvariation and positive with interclutch variation in agreementwidi the hypotheses. Therefore, the use of the independent comparativemethod strengthens the hypothesis that the evolution of eggpatterns in hosts is associated with different stages of coevolutionwith the brood parasite.     

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.     

Parasitism strategy of the grey starling, Sturnus cineraceus: Selection based on host characters and nest location

The strategy used by the intraspecific brood parasite, the grey starling, Sturnus cineraceus (Temminck) and the degree to which this strategy reflected the sources of mortality for parasite eggs were examined. Approximately 74% of all parasite eggs failed to produce young that survived to fledglings. Most of this mortality was due to two factors: (i) laying in a nest that had been deserted by a host during its nesting cycle (19%); and (ii) mismatched timing of laying in the hosts nesting cycle (38%). It is important for parasites to select a suitable host in order to avoid this mortality and increase their reproductive success. However, grey starlings did not select hosts on the basis of nest location, host characteristics, or laying date. Lack of attention to these factors implies a failure on the part of the grey starlings to recognize cues that could direct them to select host nests that would provide the best environment for their eggs. Although some egg loss and egg replacement occurred before clutch initiation by hosts, no evidence was found that parasitic birds removed host eggs after clutch initiation by hosts. These results suggest that parasites did not adopt a successful strategy for enhancing the survival rate of their own eggs.     

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, whereas 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 are 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, whereas 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.     

Ultraviolet and green parts of the colour spectrum affect egg rejection in the song thrush (Turdus philomelos)

Much attention has been devoted to understanding the evolution of egg mimicry in avian brood parasites. The majority of studies have been based on human perception when scoring the mimicry of the parasitic egg. Surprisingly, there has been no detailed study on the recognition and sensitivity towards differently coloured parasitic eggs. We investigated effect of different colours of the experimental eggs measured by ultraviolet (UV)-visible reflectance spectrophotometry on rejection behaviour in the song thrush ( Turdus philomelos ). We carried out a set of experiments with four blue model eggs representing mimetic eggs, whereas six other colours represented nonmimetic eggs. Our results revealed that two colours originally designed as a mimetic were rejected at a high rate, whereas one group of the nonmimetic was accepted. A multiple regression model of absolute differences between song thrush and experimental eggs on rejection rate showed that the level of mimicry in the UV and green parts of the colour spectrum significantly influenced egg rejection in the song thrush. To our knowledge, this is the first detailed study showing that different colour perception by the birds can affect their responses towards the parasitic egg. These findings suggest that the combination of UV and visible ranges of the spectra plays a major role in the evolution of discrimination processes, as well as in the evolution of the mimicry of the parasitic egg.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 269–276.     

The effect of Jacobin Cuckoo Clamator jacobinus parasitism on the body mass and survival of young in a new host species

The southern African subspecies of Jacobin Cuckoo Clamator jacobinus serratus is a brood parasite of a range of host species. While Jacobin Cuckoos do not evict host young, previous research has found that host young rarely survive the nestling period. Here we provide the first records of Jacobin Cuckoo parasitism of a new host species, the Southern Pied Babbler Turdoides bicolor. We investigate rates of brood parasitism and the survival of host young. The Southern Pied Babbler is one of the largest recorded hosts for Jacobin Cuckoos and, unusually, we find that host young tend to survive the nestling period and maintain similar body mass to host young in unparasitized broods. However, host young were less likely to survive to independence than young raised in unparasitized nests, suggesting a post‐fledging reproductive cost to hosts.     

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

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

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

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

Discrimination and ejection of eggs and nestlings by the fan-tailed gerygone from New Caledonia

Nestling rejection is a rare type of host defense against brood parasitism compared with egg rejection. Theoretically, host defenses at both egg and nestling stages could be based on similar underlying discrimination mechanisms but, due to the rarity of nestling rejector hosts, few studies have actually tested this hypothesis. We investigated egg and nestling discrimination by the fan-tailed gerygone Gerygone flavolateralis, a host that seemingly accepts nonmimetic eggs of its parasite, the shining bronze-cuckoo Chalcites lucidus, but ejects mimetic parasite nestlings. We introduced artificial eggs or nestlings and foreign gerygone nestlings in gerygone nests and compared begging calls of parasite and host nestlings. We found that the gerygone ejected artificial eggs only if their size was smaller than the parasite or host eggs. Ejection of artificial nestlings did not depend on whether their color matched that of the brood. The frequency of ejection increased during the course of the breeding season mirroring the increase in ejection frequency of parasite nestlings by the host. Cross-fostered gerygone nestlings were frequently ejected when lacking natal down and when introduced in the nest before hatching of the foster brood, but only occasionally when they did not match the color of the foster brood. Begging calls differed significantly between parasite and host nestlings throughout the nestling period. Our results suggest that the fan-tailed gerygone accepts eggs within the size range of gerygone and cuckoo eggs and that nestling discrimination is based on auditory and visual cues other than skin color. This highlights the importance of using a combined approach to study discrimination mechanisms of hosts.     

Comparison of digestive efficiency in the parasitic great spotted cuckoo and its magpie host nestlings

Altricial nestlings are under strong selection pressures to optimize digestive efficiency because this is one of the main factors affecting nestling growth and survival. Bird species vary in their ability to assimilate different nutrients and current theory predicts that nestlings should also be able to adjust their nutritional physiology to feeding frequency. Variation in parental provisioning to nestlings would select for flexibility in nestling digestive physiology, which would allow maximization of nutrient assimilation. In the present study, by making use of a brood parasite–host study system in which great spotted cuckoo nestlings (Clamator glandarius) are reared by magpie (Pica pica) host foster parents when sharing the nest with host nestlings, we tested several predictions of the adaptive digestive efficiency paradigm. A hand‐feeding experiment was employed in which we fed both great spotted cuckoo and magpie nestlings with exactly the same diet simulating one food abundance period and one food deprivation period. The results obtained show that cuckoo nestlings ingested more food, gained significantly more weight during the abundance period, and assimilated a higher proportion of the ingested food than magpie nestlings. These results demonstrate for the first time that cuckoo nestlings enjoy digestive adaptations that favour a rapid processing of the ingested food, thereby maximizing their intake rate but without decreasing digestive efficiency. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 280–289.     

Incubation and embryonic development affect the color of eggs of Mountain Bluebirds

Technological and theoretical advances over the past two decades have allowed researchers to quantify eggshell color in ways that were not previously possible. However, differences among studies in the timing of color measurements during laying or incubation and inclusion of data from inviable eggs may affect the results of these studies as well as conclusions based on comparisons among studies. To determine the effect of the timing of color measurements, we compared the color of the eggs of Mountain Bluebirds (Sialia currucoides) during both laying/early incubation and late incubation. We also assessed the influence of egg viability on eggshell color by comparing viable and inviable eggs from the same clutch. We found that all color metrics investigated (blue‐green and UV chroma, brightness, and hue) were significantly different between early and late incubation, and viable and inviable eggs. However, color metrics of eggs measured during early and late incubation and of viable and inviable eggs in the same clutch were correlated. Our results suggest that the timing of color measurements and the viability of eggs have important effects on eggshell color and, therefore, in future studies, investigators should always provide information about the timing of measurements and the viability of eggs measured. Our results also suggest that comparisons among studies where eggshell color was measured at different times and/or the viability of eggs was not determined or reported are possible, given that the color metrics of viable and inviable eggs and of eggs measured at different times in our study were correlated, but those comparisons should be interpreted with caution.