Ectoparasite Activity During Incubation Increases Microbial Growth on Avian Eggs.

While direct detrimental effects of parasites on hosts are relatively well documented, other more subtle but potentially important effects of parasitism are yet unexplored. Biological activity of ectoparasites, apart from skin injuries and blood-feeding, often results in blood remains, or parasite faeces that accumulate and modify the host environment. In this way, ectoparasite activities and remains may increase nutrient availability that may favour colonization and growth of microorganisms including potential pathogens. Here, by the experimental addition of hematophagous flies (Carnus hemapterus, a common ectoparasite of birds) to nests of spotless starlings Sturnus unicolor during incubation, we explore this possible side effect of parasitism which has rarely, if ever, been investigated. Results show that faeces and blood remains from parasitic flies on spotless starling eggshells at the end of incubation were more abundant in experimental than in control nests. Moreover, eggshell bacterial loads of different groups of cultivable bacteria including potential pathogens, as well as species richness of bacteria in terms of Operational Taxonomic Units (OTUs), were also higher in experimental nests. Finally, we also found evidence of a link between eggshell bacterial loads and increased embryo mortality, which provides indirect support for a bacterial-mediated negative effect of ectoparasitism on host offspring. Trans-shell bacterial infection might be one of the main causes of embryo death and, consequently, this hitherto unnoticed indirect effect of ectoparasitism might be widespread in nature and could affect our understanding of ecology and evolution of host-parasite interactions.

Hoopoes color their eggs with antimicrobial uropygial secretions.

Uropygial gland secretions are used as cosmetics by some species of birds to color and enhance properties of feathers and teguments, which may signal individual quality. Uropygial secretions also reach eggshells during incubation and, therefore, may influence the coloration of birds' eggs, a trait that has attracted the attention of evolutionary biologists for more than one century. The color of hoopoe eggs typically changes along incubation, from bluish-gray to greenish-brown. Here, we test experimentally the hypothesis that dark uropygial secretion of females is responsible for such drastic color change. Moreover, since uropygial secretion of hoopoes has antimicrobial properties, we also explore the association between color and antimicrobial activity of the uropygial secretion of females. We found that eggs stayed bluish-gray in nests where female access to the uropygial secretion was experimentally blocked. Furthermore, experimental eggs that were maintained in incubators and manually smeared with uropygial secretion experienced similar color changes that naturally incubated eggs did, while control eggs that were not in contact with the secretions did not experience such color changes. All these results strongly support the hypothesis that female hoopoes use their uropygial gland secretion to color the eggs. Moreover, saturation of the uropygial secretion was associated with antimicrobial activity against Bacillus licheniformis. Given the known antimicrobial potential of uropygial secretions of birds, this finding opens the possibility that in scenarios of sexual selection, hoopoes in particular and birds in general signal antimicrobial properties of their uropygial secretion by mean of changes in egg coloration along incubation.

Does avian conspicuous colouration increase or reduce predation risk?

Animals often announce their unprofitability to predators through conspicuous coloured signals. Here we tested whether the apparently conspicuous colour designs of the four European Coraciiformes and Upupiformes species may have evolved as aposematic signals, or whether instead they imply a cost in terms of predation risk. Because previous studies suggested that these species are unpalatable, we hypothesized that predators could avoid targeting them based on their colours. An experiment was performed where two artificial models of each bird species were exposed simultaneously to raptor predators, one painted so as to resemble the real colour design of these birds, and the other one painted using cryptic colours. Additionally, we used field data on the black kite's diet to compare the selection of these four species to that of other avian prey. Conspicuous models were attacked in equal or higher proportions than their cryptic counterparts, and the attack rate on the four species increased with their respective degree of contrast against natural backgrounds. The analysis of the predator's diet revealed that the two least attacked species were negatively selected in nature despite their abundance. Both conspicuous and cryptic models of one of the studied species (the hoopoe) received fewer attacks than cryptic models of the other three species, suggesting that predators may avoid this species for characteristics other than colour. Globally, our results suggest that the colour of coraciiforms and upupiforms does not function as an aposematic signal that advises predators of their unprofitability, but also that conspicuous colours may increase predation risk in some species, supporting thus the handicap hypothesis.

The evolution of size of the uropygial gland: mutualistic feather mites and uropygial secretion reduce bacterial loads of eggshells and hatching failures of European birds.

Potentially, pathogenic bacteria are one of the main infective agents against which a battery of chemical and physical barriers has evolved in animals. Among these are the secretions by the exocrine uropygial gland in birds. The antimicrobial properties of uropygial secretions may prevent colonization and growth of microorganisms on feathers, skin and eggshells. However, uropygial gland secretions also favour the proliferation of feather mites that feed on secretions and microorganisms living on feathers that would otherwise reach eggshells during incubation if not consumed by feather mites. Therefore, at the interspecific level, uropygial gland size (as an index of volume of uropygial secretion) should be positively related to eggshell bacterial load (i.e. the risk of egg infection), whereas eggshell bacterial loads may be negatively related to abundance of feather mites eating bacteria. Here, we explore these previously untested predictions in a comparative framework using information on eggshell bacterial loads, uropygial gland size, diversity and abundance of feather mites and hatching success of 22 species of birds. The size of the uropygial gland was positively related to eggshell bacterial loads (mesophilic bacteria and Enterobacteriaceae), and bird species with higher diversity and abundance of feather mites harboured lower bacterial density on their eggshells (Enterococcus and Staphylococcus), in accordance with the hypothesis. Importantly, eggshell bacterial loads of mesophilic bacteria, Enterococcus and Enterobacteriaceae were negatively associated with hatching success, allowing us to interpret these interspecific relationships in a functional scenario, where both uropygial glands and mutualistic feather mites independently reduce the negative effects of pathogenic bacteria on avian fitness.

Rapid change in host use of the common cuckoo Cuculus canorus linked to climate change.

Parasites require synchrony with their hosts so if host timing changes with climate change, some parasites may decline and eventually go extinct. Residents and short-distance migrant hosts of the brood parasitic common cuckoo, Cuculus canorus, have advanced their phenology in response to climate change more than long-distance migrants, including the cuckoo itself. Because different parts of Europe show different degrees of climate change, we predicted that use of residents or short-distance migrants as hosts should have declined in areas with greater increase in spring temperature. Comparing relative frequency of parasitism of the two host categories in 23 European countries before and after 1990, when spring temperatures in many areas had started to increase, we found that relative parasitism of residents and short-distance migrants decreased. This change in host use was positively related to increase in spring temperature, consistent with the prediction that relative change in phenology for different migrant classes drives host-use patterns. These findings are consistent with the hypothesis that climate change affects the relative abundance of different host races of the common cuckoo.

Symbiotic bacteria living in the hoopoe's uropygial gland prevent feather degradation.

Among potential agents that might damage bird feathers are certain microorganisms which secrete enzymes that digest keratin, as is the case of the ubiquitous bacterium Bacillus licheniformis, present in both the feathers and skin of wild birds. It is therefore a good candidate for testing the effects of bird defences against feather-degrading microorganisms. One of these defences is the oil secreted by the uropygial gland, which birds use to protect their feathers against parasites. In previous studies we have shown how Enterococcus faecalis strains isolated from nestling hoopoes exert antagonistic effects against B. licheniformis, mediated by the production of bacteriocins. Consequently we hypothesized that this enterococcus and the bacteriocins it engenders might act as a defence against feather-degrading microorganisms in hoopoes. We investigated this hypothesis in a series of laboratory experiments and evaluated the extent to which the keratinolytic effects caused by B. licheniformis were reduced by the E. faecalis MRR10-3 strain, isolated from hoopoes, and its bacteriocins. In different treatments, feathers or pure keratin was incubated with B. licheniformis, B. licheniformis together with E. faecalis MRR10-3, and B. licheniformis together with the bacteriocins produced by E. faecalis MRR10-3. Our results were in accordance with the predicted effects on hoopoe feathers. There was a significant decrease both in pure keratin loss and in feather degradation in the presence of the symbiotic bacterium or its bacteriocin. These results suggest that by preening their feathers hoopoes benefit from their symbiotic relationship with bacteriocin-producing enterococci, which constitute a chemical defence against feather degradation.

Parasitism, host immune defence and dispersal.

Host-parasite interactions have been hypothesized to affect the evolution of dispersal by providing a possibility for hosts to escape debilitating parasites, and by influencing the level of local adaptation. We used a comparative approach to investigate the relationship between a component of host immune function (which reflects the evolutionary history of parasite-induced natural selection) and dispersal in birds. We used a sample of 46 species of birds for which we had obtained field estimates of T-cell response for nestlings, mainly from our own field studies in Denmark and Spain. Bird species with longer natal, but not with longer breeding dispersal distances had a stronger mean T-cell-mediated immune response in nestlings than species with short dispersal distances. That was also the case when controlling for the potentially confounding effect of migration from breeding to wintering area, which is known from previous studies to be positively associated with dispersal distance. These relationships held even when controlling for similarity among species because of common ancestry. Avian hosts with a larger number of different breeding habitats had weaker mean T-cell-mediated immune responses than habitat specialists. This relationship held even when controlling for similarity among species because of common ancestry. Therefore, T-cell-mediated immunity is an important predictor of evolutionary changes in dispersal ability among common European birds.

Females are responsible for ejection of cuckoo eggs in the rufous bush robin.

Rufous bush robin, Cercotrichas galactotes, nests were experimentally parasitized in order to test which sex is responsible for egg ejection. We tested nests belonging to the same individuals (male, female or pair) in 2 consecutive years. Whether the eggs were rejected did not depend on environmental variables such as laying date and clutch size, and did not change between tests, when the two consecutive nests tested belonged to the same pair members, supporting the idea that some individuals reject odd eggs, while others accept them. The expected frequencies for rejection and acceptance, if females were the sex responsible for ejection behaviour, did not differ from the observed frequencies when the same female owned both the nests tested. However, the expected frequencies calculated for males as if they were the sex responsible differed from those observed, when the same male owned both the nests tested. A lower percentage of females than males changed ejection behaviour. These results show that female rufous bush robins are responsible for egg ejection. Copyright 1998 The Association for the Study of Animal Behaviour.