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Bacteria have been suggested as being partially responsible for avian nest odours and, thus, volatiles from their metabolism could influence the intensity of selection pressures due to parasites detecting olfactory cues of their hosts. Here, we tested this hypothesis by exploring intraspecific and interspecific variability in microbial environments, volatile profiles and intensity of ectoparasitism by Carnus hemapterus in the nests of 10 avian species. As expected, we found that (i) alpha and beta diversity of microbial and volatile profiles were associated with each other. Moreover, (ii) alpha diversity of bacteria and volatiles of the nest environment, as well as some particular bacteria and volatiles, was associated with the intensity of parasitism at early and late stages of the nestling period. Finally, (iii) alpha diversity of the nest microbiota, as well as some particular bacteria and volatiles, was correlated with fledging success. When considering them together, the results support the expected links between the microbial environment and nest odours in different bird species, and between the microbial environment and both ectoparasitism intensity and fledging success. Relative abundances of particular volatiles and bacteria predicted ectoparasitism and/or fledging success. Future research should prioritise experimental approaches directed to determine the role of bacteria and volatiles in the outcomes of host-ectoparasite interactions., (© The Author(s) 2024. Published by Oxford University Press on behalf of FEMS.)

Mutualistic symbioses between animals and bacteria depend on acquisition of appropriate symbionts while avoiding exploitation by non-beneficial microbes. The mode of acquisition of symbionts would determine, not only the probability of encountering but also evolutionary outcomes of mutualistic counterparts. The microbiome inhabiting the uropygial gland of the European hoopoe (Upupa epops) includes a variety of bacterial strains, some of them providing antimicrobial benefits. Here, the mode of acquisition and stability of this microbiome is analyzed by means of Automated rRNA Intergenic Spacer Analysis and two different experiments. The first experiment impeded mothers' access to their glands, thus avoiding direct transmission of microorganisms from female to offspring secretions. The second experiment explored the stability of the microbiomes by inoculating glands with secretions from alien nests. The first experiment provoked a reduction in similarity of microbiomes of mother and nestlings. Interestingly, some bacterial strains were more often detected when females had not access to their glands, suggesting antagonistic effects among bacteria from different sources. The second experiment caused an increase in richness of the microbiome of receivers in terms of prevalence of Operational Taxonomic Units (OTUs) that reduced differences in microbiomes of donors and receivers. That occurred because OTUs that were present in donors but not in receivers incorporated to the microbiome of the latter, which provoked that cross-inoculated nestlings got similar final microbiomes that included the most prevalent OTUs. The results are therefore consistent with a central role of vertical transmission in bacterial acquisition by nestling hoopoes and support the idea that the typical composition of the hoopoe gland microbiome is reached by the incorporation of some bacteria during the nestling period. This scenario suggests the existence of a coevolved core microbiome composed by a mix of specialized vertically transmitted strains and facultative symbionts able to coexist with them. The implications of this mixed mode of transmission for the evolution of the mutualism are discussed.

Host defences against cuckoo parasitism and cuckoo trickeries to overcome them are a classic example of antagonistic coevolution. Recently it has been reported that this relationship may turn to be mutualistic in the case of the carrion crow (Corvus corone) and its brood parasite, the great spotted cuckoo (Clamator glandarius), given that experimentally and naturally parasitized nests were depredated at a lower rate than non-parasitized nests. This result was interpreted as a consequence of the antipredatory properties of a fetid cloacal secretion produced by cuckoo nestlings, which presumably deters predators from parasitized host nests. This potential defensive mechanism would therefore explain the detected higher fledgling success of parasitized nests during breeding seasons with high predation risk. Here, in a different study population, we explored the expected benefits in terms of reduced nest predation in naturally and experimentally parasitized nests of two different host species, carrion crows and magpies (Pica pica). During the incubation phase non-parasitized nests were depredated more frequently than parasitized nests. However, during the nestling phase, parasitized nests were not depredated at a lower rate than non-parasitized nests, neither in magpie nor in carrion crow nests, and experimental translocation of great spotted cuckoo hatchlings did not reveal causal effects between parasitism state and predation rate of host nests. Therefore, our results do not fit expectations and, thus, do not support the fascinating possibility that great spotted cuckoo nestlings could have an antipredatory effect for host nestlings, at least in our study area. We also discuss different possibilities that may conciliate these with previous results, but also several alternative explanations, including the lack of generalizability of the previously documented mutualistic association.

Exploring factors guiding interactions of bacterial communities with animals has become of primary importance for ecologists and evolutionary biologists during the last years because of their likely central role in the evolution of animal life history traits. We explored the association between laying date and eggshell bacterial load (mesophilic bacteria, Enterobacteriaceae, Staphylococci, and Enterococci) in natural and artificial magpie (Pica pica) nests containing fresh commercial quail (Coturnix coturnix) eggs. We manipulated hygiene conditions by spilling egg contents on magpie and artificial nests and explored experimental effects during the breeding season. Egg breakage is a common outcome of brood parasitism by great spotted cuckoos (Clamator glandarius) on the nests of magpie, one of its main hosts. We found that the treatment increased eggshell bacterial load in artificial nests, but not in magpie nests with incubating females, which suggests that parental activity prevents the proliferation of bacteria on the eggshells in relation to egg breakage. Moreover, laying date was positively related to eggshell bacterial load in active magpie nests, but negatively in artificial nests. The results suggest that variation in parental characteristics of magpies rather than climatic variation during the breeding season explained the detected positive association. Because the eggshell bacterial load is a proxy of hatching success, the detected positive association between eggshell bacterial loads and laying date in natural, but not in artificial nests, suggests that the generalized negative association between laying date and avian breeding success can be, at least partially, explained by differential bacterial effects.

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., (© 2014 The Authors. Journal of Evolutionary Biology © 2014 European Society For Evolutionary Biology.)

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

Predator-prey and host-parasite interactions and mutualisms are common and may have profound effects on ecosystems. Here we analyze the parasitic and mutualistic associations between three groups of organisms: the plant Artemisia maritima, bacteria, and a colonial seabird (the sandwich tern Sterna sandvicensis) that breeds in dense colonies covered in feces produced by both adults and chicks. A disproportionately large fraction of colonies of the sandwich tern in Denmark were located in patches covered by A. maritima. This association was specific for the densely colonial sandwich tern, but was not present for four other sympatric species of terns that breed in much less dense colonies. A. maritima reduced the abundance of pathogenic Staphylococcus on chicken eggshells in a field experiment. Recruitment by sandwich terns breeding in patches of A. maritima was 18 % higher than for sandwich terns breeding in the absence of A. maritima. A. maritima benefitted from the association with sandwich terns due to the supply of nutrients from feces and uneaten food lost by young. These findings are consistent with sandwich terns exploiting the association with A. maritima and its antimicrobial properties to improve their reproductive success, while sandwich terns and A. maritima are involved in a mutualistic interaction.

Environmental characteristics of neighboring locations are generally more similar than those of distant locations. Selection pressures due to parasitism and other environmental conditions shape life history traits of hosts; thus, the probability of parasitism should be associated with the strength of spatial autocorrelation in life history and defensive traits of their hosts. Here we test this hypothesis in three different subpopulations of Magpie (Pica pica) parasitized by the Great Spotted Cuckoo (Clamator glandarius) during three breeding seasons. In some of the years and study plots, we found evidence of positive spatial autocorrelations for clutch size and parasitism rate, but not for laying date. As predicted, brood parasitism was associated with the strength of these spatial autocorrelations. Magpies that bred close to each other in areas of high risk of parasitism responded similarly to experimental parasitic eggs. Moreover, an elevated risk of parasitism eliminated the spatial autocorrelation for clutch size, which became randomly distributed. We discuss possible mechanisms explaining these associations, which may have important consequences for estimating evolutionary responses of hosts to parasitic infections and, therefore, for epidemiological, ecological, and evolutionary studies of host-parasite relationships.

Wallace proposed in 1868 that natural rather than sexual selection could explain the striking differences in avian plumage dichromatism. Thus, he predicted that nesting habits, through their association with nest predation, could drive changes in sexual dichromatism by enabling females in cavity nesters to become as conspicuous as males, whereas Darwin (1871, The Descent of Man and Selection in Relation to Sex, John Murray, London) argued that sexual selection was the sole explanation for dichromatism. Sexual dichromatism is currently used as indicating the strength of sexual selection, and therefore testing Wallace's claim with modern phylogentically controlled methodologies is of prime interest for comparing the roles of natural and sexual selection in affecting the evolution of avian coloration. Here, we have related information on nest attendance, sexual dichromatism and nesting habits (open and cavity nesting) to male and female plumage conspicuousness in European passerines. Nest incubation attendance does not explain male or female plumage conspicuousness but nest type does. Moreover, although females of monochromatic and cavity nesting species are more conspicuous than females of other species, males of monochromatic and open nesting species are those with more cryptic plumage. Finally, analyses of character evolution suggest that changes in nesting habits influence the probability of changes in both dichromatism and plumage conspicuousness of males but do not significantly affect those in females. These results strongly suggest a role of nesting habits in the evolution of plumage conspicuousness of males, and a role for sexual selection also in females, both factors affecting the evolution of sexual dichromatism. We discuss our findings in relation to the debate that Darwin and Wallace maintained more than one century ago on the importance of natural and sexual selection in driving the evolution of plumage conspicuousness and sexual dichromatism in birds, and conclude that our results partly support the evolutionary scenarios envisaged by both extraordinary scientists., (© 2012 The Authors. Journal of Evolutionary Biology © 2012 European Society For Evolutionary Biology.)

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

Several experimental results support the existence of costs associated with exaggerated begging behaviour, which are assumed by some theoretical models of honest signalling in parent-offspring communication. However, to understand how honest begging behaviour is evolutionarily maintained in nature, the long-term cost-benefit output associated with exaggerated signals should also be estimated. As far as we know, the net cost-benefit balance of begging display has not previously been explored. Here, we used an appetite stimulant, cyproheptadine hydrochloride, to increase the feeling of hunger in some magpie nestlings. Supporting the use of cyproheptadine to manipulate hunger level and thereby begging behaviour, we found that experimental nestlings increased the frequency of begging and received more food than their control nestmates. Contrary to the expectation that physiological costs per se counteract the associated benefits of escalated begging signals, we found that near-fledging experimental magpies showed a better physical condition than control nestlings. These findings stress the interesting question of why magpie nestlings do not show to adults an escalated level of hunger if it implies an advantage. We discuss the responsibility of inclusive fitness costs and indirect genetic effects for the maintenance of honesty in parent-offspring communication.

Background: Nestlings of altricial birds capture parents' attention through conspicuous visual displays, including exposure of their gape coloration which informs parents about their level of need, competitive ability or health; information that parents use for deciding food allocation among their offspring. Thus, because nestlings compete with nest mates for parental care, nestling conspicuousness is expected to increase with level of sibling competition along bird phylogeny., Methodology/principal Findings: We test this prediction by jointly using information of brood reduction, clutch size and duration of nestling period as proxies for intensity of sibling competition, and visual models that assess detectability of nestlings by adult birds. As predicted, we found a positive association between nestling conspicuousness and intensity of brood reduction, while clutch size and duration of nestling period did not enter in the best models. Level of brood reduction was positively related with the achromatic component of nestling conspicuousness and body mass was negatively related with the chromatic component., Conclusions: These associations are in agreement with the hypothesis that sibling competition for parental attention has driven the evolution of visual nestling conspicuousness in a context of parent-offspring communication in altricial birds.

A considerable number of bird species carry feathers to their nests. Feathers' presence in the nests has traditionally been explained by their insulating properties. Recently, however, it has been suggested that feathers carried to the nests by females of the spotted starling (Sturnus unicolor L.) could have an ornamental function based on their ultraviolet (300-400 nm) and human-visible longer wavelength (400-700 nm) coloration. In our population, 95.7% of feathers found inside next-boxes occupied by nesting starlings were rock dove fly feathers. Of these feathers, 82.7% were naturally positioned with their reverse side oriented toward the entrance hole and 42.4% of all found feathers were situated within the nest-cup. Here we experimentally assess the signaling function of ultraviolet coloration of feathers in nests of spotless starlings by providing nests with a number of pigeon flight feathers that were respectively treated on their obverse, reverse, both, or neither side with a UV blocker. Starlings placed 42.5% of the experimental feathers in the nest-cup irrespective of the UV block treatment. Orientation of feathers toward the entrance hole was not related with their ultraviolet radiation. However, feathers placed within the nest-cup were more likely found with their reverse side oriented toward the entrance hole confirming our correlative findings. These results suggest a minor role of ultraviolet coloration on feather location by spotless starlings.

Nests of altricial birds exhibit variable spectral properties that may affect the efficacy (conspicuousness) of the colored begging traits that a nestling displays to its parents. Here we explored whether selection for efficient perception has favored the evolution of nestling color designs that maximizes nestling detectability in variable light environments. Visual models were used to estimate how parents perceive the coloration of mouths, flanges, heads, and breasts of nestlings within their nest in 21 species of European birds. We show that the largest chromatic and achromatic contrasts against the nest background appeared for nestling mouths and flanges, respectively. Nestlings of open-nesting species showed a larger general achromatic contrast with the nest than did nestlings of hole-nesting species. However, nestlings of hole nesters showed a more evident achromatic contrast between flanges and other traits than did nestlings of open nesters. In addition, species with larger clutch sizes showed larger general achromatic contrasts with the nest. Gaping traits of open-nesting species contrasting with the nest background were better perceived under rich light regimes than under poor ones. These findings are consistent with a scenario in which selection for nestling detectability in dark environments has favored the evolution of particular achromatic components of gape coloration but also nestling traits that enhance signal efficacy by maximizing color contrasts within a nestling.

The level of defense against great spotted cuckoo (Clamator glandarius) parasitism in different European populations of magpie (Pica pica) depends on selection pressures due to parasitism and gene flow between populations, which suggests the existence of coevolutionary hot spots within a European metapopulation. A mosaic of coevolution is theoretically possible at small geographical scales and with strong gene flow, because, among other reasons, plots may differ in productivity (i.e., reproductive success of hosts in the absence of parasitism) and defensive genotypes theoretically should be more common in plots of high productivity. Here, we tested this prediction by exploring the relationship between parasitism rate, level of defense against parasitism (estimated as both rejection rate and the frequency of the 457bp microsatellite allele associated with foreign egg rejection in magpies), and some variables related to the productivity (average laying date, clutch size, and number of hatchlings per nest) of magpies breeding in different subpopulations. We found that both estimates of defensive ability (egg rejection rate and frequency of the 457bp allele) covaried significantly with between-plot differences in probability of parasitism, laying date, and number of hatchlings per nest. Moreover, the parasitism rate was larger in more productive plots. These results confirm the existence of a mosaic of coevolution at a very local geographical scale, and the association between laying date and number of hatchlings with variables related to defensive ability and the selection pressure arising from parasitism supports the prediction of coevolutionary gradients in relation to host productivity.

Owing to the conspicuousness of ultraviolet (UV) colour in dark environments, natural selection might have selected UV egg coloration because it would enhance egg detectability by parents in murky nests. Here, we tested this hypothesis by using comparative and experimental approaches. First, we studied variation in egg coloration of 98 species of European passerines measured using UV-visible reflectance spectrometry (300-700nm) in relation to nesting habits. Analyses based on raw data and controlling for phylogenetic distances both at the species and the family levels revealed that hole-nester species produced eggs with higher UV reflectance than those nesting in open habitats. The experimental approach consisted of the manipulation of UV reflectance of the experimental eggs introduced outside the nest-cup of the hole-nester spotless starling Sturnus unicolor and the study of the retrieval of these eggs. Ultraviolet-reflecting eggs (controls) were more frequently retrieved to the nest-cup than non-reflecting (-UV) eggs. These results were not due to '-UV' eggs being recognized by starlings as parasitic because when a parasitic egg is detected, starlings removed it from the nest-box. Therefore, these results are consistent with the hypothesis that UV egg colours are designed to provide highly detectable targets for parent birds in dark nest environments.

Among several adaptive explanations proposed to account for variation in avian egg color, that related to sexual selection is of particular interest because of its possible generality. Briefly, it proposes that because biliverdin (the pigment responsible for blue-green eggshell coloration) is an antioxidant, deposition in the eggshell by laying females may signal the capacity of females to control free radicals, despite the handicap of removing this antioxidant from their body. If males adjust parental effort in response to the intensity of the blue coloration of eggs, thereby investing more in the offspring of high-quality mates, blue eggs may represent a postmating sexually selected signal in females. Here, by image and spectrophotometric analyses of the eggs of European passerines, we tested two different predictions of the hypothesis. First, variables related to intraspecific variation in parental effort (i.e., the duration of the nestling period controlled for body mass) should be positively related to the intensity of blue-green color of the eggshell across species. Second, there should be a positive relationship between intensity of blue-green color of eggs and degree of polygyny. These predictions were supported: intensity of blue-green coloration (i.e., chroma) was significantly related to the duration of the nestling period and to degree of polygyny after controlling for possible confounding variables (i.e., body mass, incubation period, and nest type) and similarity due to common descent. Nest type (hole or nonhole) also explained a significant proportion of variation in egg chroma, perhaps reflecting different selection pressures (i.e., light conditions, risk of parasitism) affecting species with the two types of nests.