Jesús M. Avilés

Dark nests and egg colour in birds: a possible functional role of ultraviolet reflectance in egg detectability

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 (300–700u200anm) 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.

Experimental support for the use of egg uniformity in parasite egg discrimination by cuckoo hosts

Common cuckoo (Cuculus canorus) parasitism drastically reduces the reproductive success of their hosts and selects for host discrimination of cuckoo eggs. In a second stage of anti-parasite adaptation, once cuckoos can lay eggs that mimic those of their hosts, a high uniformity of host egg appearance within a clutch may favour cuckoo egg discrimination. Comparative evidence provides indirect support for this hypothesis although experimental support is currently lacking. Here, we studied the effect of experimentally decreased uniformity of host egg appearance on cuckoo egg discrimination by great reed warbler (Acrocephalus arundinaceus) hosts in a population in which long-term cuckoo parasitism has led to high levels of cuckoo–host egg mimesis. We manipulated host clutch uniformity by adding extra spots to fresh host eggs just after they were laid. Rejection of non-mimetic experimental eggs added to these nests was compared with those in control nests in which uniformity was not altered. Previously, by over-painting real spots in a control group of nests, we showed a negligible effect of our paints on hosts’ perception of their eggs. We show that for the great reed warbler, non-mimetic experimental eggs were relatively more tolerated in experimental nests, i.e. with lower uniformity (40%) than in control nests (5%). This is the first experimental study, to our knowledge, which demonstrates a reduced discrimination of foreign eggs as a consequence of an increase of egg phenotypes variation perception in a cuckoo host.

Increased host tolerance of multiple cuckoo eggs leads to higher fledging success of the brood parasite

In birds, multiple parasitism is the laying of two or more eggs by one or more parasitic females in a single host nest. Several cognitive mechanisms may explain how multiple parasitism could affect parasite egg discrimination by hosts. Rejection based on discordance predicts that multiple parasitism provides a perceptually more error-prone way for hosts to reject parasitism because more foreign eggs decrease the chance that any one egg is perceived as most dissimilar and recognized as foreign, unless parasite eggs are all similarly highly nonmimetic. In contrast, rejection based on clutch uniformity predicts that in multiple parasitism egg rejection is more error-proof if mimicry by parasite eggs is variable, because increased variation in egg appearance makes for easier egg rejection for hosts. Finally, true egg recognition, that is, rejection based on memory of the hosts own eggs, predicts no differences in rejection rates from nests with single or multiple parasitism. We studied common cuckoos, Cuculus canorus, parasitizing a population of great reed warblers, Acrocephalus arundinaceus, in Hungary where multiple parasitism was frequent. Hosts rejected parasite eggs less often in nests with multiple parasitism than in nests with single parasitism. These observations were confirmed by experimental parasitism and support the rejection based on discordance hypothesis. As hosts were more likely to tolerate cuckoo eggs in nests with multiple parasitism, we found that multiple parasitism more than doubled cuckoos reproductive output per host nest compared to single parasitism.

Beak colour reflects circulating carotenoid and vitamin A levels in spotless starlings (Sturnus unicolor)

Many colourful sexually selected signals in animals are carotenoid-dependent and, because carotenoids function as antiradicals and immunostimulating molecules, carotenoid-dependent signals may honestly reflect the health state of individuals. Some others nutrients like vitamin A may also enhance health and colouration, but these have rarely been tested alongside carotenoids in colourful birds. Here, we examined whether beak colour of the spotless starling (Sturnus unicolor) reflected circulating levels of carotenoids and/or vitamin A (retinol). Spotless starlings are polygynous, sexually dimorphic birds (i.e. length of chest feathers). The tip of the beaks of male and female spotless starlings is more intensely coloured at the beginning of the breeding season and becomes dull after mating, which may suggest a sexual function. We found that females have a more intensely coloured beak and higher plasma carotenoid concentration than males during mating, and, despite the finding that carotenoid and vitamin A levels were not significantly related; colour intensity was positively correlated with plasma concentration of carotenoids and vitamin A in both sexes. However, adult beak coloration was not associated with carotenoid and vitamin A concentrations after nestlings were hatched. Therefore, beak colouration of spotless starlings provides information about circulating levels of carotenoids and vitamins during the mating season and may potentially function as a reliable signal of physiological status in the context of sexual selection.

Male spotless starlings adjust feeding effort based on egg spots revealing ectoparasite load

Parents may vary their parental behaviour and investment in reproduction in response to parasite-induced changes in the fitness prospects of their offspring. Thus, parents may use the physical condition of their offspring, or any other trait related to parasite load, to adjust parental effort. The immaculate eggs of the spotless starling, Sturnus unicolor , often become densely spotted owing to the activity of the ectoparasite carnid fly Carnus hemapterus . Spot density anticipates the intensity of fly infestation suffered by nestlings and, therefore, may serve as a cue for parents to adjust reproductive investment. By cleaning spots produced by C. hemapterus on eggs of spotless starlings, we manipulated the parasites traces revealing its presence in broods of starlings, without modifying the level of infestation, to test whether parents use these signals to adjust reproductive effort. We found support for the hypothetical negative effect of Carnus flies since nestlings raised in nests with a higher fly load had lower body mass. The experimental egg cleaning during incubation did not change the intensity of carnid fly infestation during nestling development. However, it had a significant positive influence on paternal but not maternal effort. Our experimental results support the idea that spotless starling males adjust their effort in response to their perception of the fitness prospects of their nestlings as indirectly estimated by traces of parasites on the eggshells. As far as we know, this is the first evidence of the use of parasite traces to infer risk of parasitic infestation by animal hosts.

Do great tits rely on inadvertent social information from blue tits? A habitat selection experiment

Sympatric species sharing requirements are competitors, but recent evidence suggests that heterospecifics may also be used as a source of information. The heterospecific habitat copying hypothesis proposes that individuals of one species might use information inadvertently produced by the breeding performance of individuals of other species to assess habitat quality whenever the two species share needs. In this study, we provide the first experimental test of this hypothesis by examining whether the manipulated reproductive success of blue tits (Cyanistes caeruleus) is used as heterospecific inadvertent social information (ISI) in breeding-habitat selection by sympatric great tits (Parus major). The reproductive success of blue tits was manipulated 1year at the scale of patches by transferring nestlings from decreased to increased patches. No evidence was found of great tits using the reproductive success of blue tits as a source of heterospecific ISI. However, dispersal decisions by adult great tits correlated with information on con- and heterospecific densities, which constitute other sources of ISI. As density and breeding performance are tightly intertwined forms of information, the difficulty in distinguishing between them might lead great tits to use heterospecific ISI more in the form of density than breeding performance when making dispersal decisions.

Informative content of multiple plumage-coloured traits in female and male European Rollers

Animals may assess the quality of other individuals by using information that different ornaments may provide. The European Roller (Coracias garrulus) is a socially monogamous species in which males and females display highly conspicuous plumage colouration. According to the mutual selection hypothesis, we predicted that, in this species, plumage coloration could signal individual quality in both sexes because both female and male rollers invest a considerable amount of time caring for their offspring. We used spectrophotometric measurements to investigate the information content of multiple plumage colour traits. We found that the roller is actually a sexually dimorphic and dichromatic species. Different plumage colours from different origins were correlated within individual. Head and back brightness correlated with body condition in both sexes, and in males, head brightness correlated with the number of fledglings in successful nests, while head green-yellow saturation correlated with parental provisioning. Meanwhile, in females, back brightness was related to the number of fledglings in successful nests and to parental provisioning rate. In addition, there was a positive assortative mating in relation to weight, body condition, head green-yellow saturation and back brightness. Finally, we found a positive correlation between parent and offspring coloration. Altogether, these results suggest that multiple colour traits may act as quality indicators in the roller and that they may be used by the two sexes to assess potential mate quality.

Alarm calls modulate the spatial structure of a breeding owl community

Animals should continuously assess the threat of predation. Alarm calls inform on predation risk and are often used as cues to shape behavioural responses in birds and mammals. Hitherto, however, the ecological consequences of alarm calls in terms of organization of animal communities have been neglected. Here, we show experimentally that calls of a resident nocturnal raptor, the little owl Athene noctua, triggered a response in terms of breeding habitat selection and investment in current reproduction in conspecifics and heterospecifics. Little owls preferred to settle in territories where calls of conspecifics, irrespective of their type (i.e. alarm versus contact calls), were broadcasted, indicating that either conspecific attraction exists or calls are interpreted as foreign calls, eliciting settlement as a mode of defence against competitors. Also, we found that little owls seemed to invest more in current reproduction in safe territories as revealed by conspecific calls. Innovatively, we reported that a second owl species, the migratory scops owl Otus scops, preferred to breed in safe territories as indicated by little owls calls. These results evidence that the emission of alarm calls may have, apart from well-known behavioural effects, ecological consequences in natural communities by inducing species-specific biases in breeding habitat selection. This study demonstrates a previously unsuspected informative role of avian alarm calls which may modulate the spatial structure of species within communities.

Experimental feeding affects the relationship between hematocrit and body mass in Spotless Starling (Sturnus unicolor) nestlings

Hematocrit, the proportion of blood volume occupied by packed red blood cells, is frequently used as an estimate of phenotypic condition. Some studies in birds, however, suggest that hematocrit might not always be a good estimate of condition. We tested the reliability of hematocrit as an estimate of condition by investigating the relationship between hematocrit and two other estimates of phenotypic condition (body mass controlled for body size and T-cell-mediated immune response) in nestlings of the Spotless Starling (Sturnus unicolor) under different environmental conditions. Half of each brood received an experimental food supplement while the other half was kept as a control. Hematocrit was positively related to relative body mass only in control nestlings whereas the relationship between hematocrit and cellular immune response was far from significant in both groups of nestlings. As expected, experimental food supply weakened the relationship between hematocrit and relative body mass, but this effect was not mediated by a decrease in the variation of phenotypic condition among nestlings. Instead, the effect of food supplementation was condition-dependent, reducing hematocrit in heavier than average nestlings, and increasing hematocrit in lighter than average nestlings. These results suggest that hematocrit might not be a reliable estimate of phenotypic condition under certain nutritional circumstances.

Eavesdropping cuckoos: further insights on great spotted cuckoo preference by magpie nests and egg colour

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.