The evolutionary ecology of bird-ant interactions: a pervasive but under-studied connection.

Birds and ants are among the most ubiquitous taxa co-occurring in terrestrial ecosystems, but how they mutually interact is almost unknown. Here, the main features of this neglected interaction are synthetized in a systematic literature review. Interaction with ants has been recorded in 1122 bird species (11.2% of extant species) belonging to 131 families widely distributed across the globe and the avian phylogeny. On the other hand, 47 genus of ants (14.4% of extant genus) belonging to eight subfamilies interact with birds. Interactions include competition, antagonism (either ant-bird mutual predation or parasitism) and living together commensally or mutualistically. Competition (48.9%) and antagonism (36.1%) were the most common reported interactions. The potential for engaging in commensalism and competition with ants has a phylogenetic structure in birds and was present in the birds' ancestor. Interaction is better studied in the tropics, in where the network is less dense and more nested than in temperate or arid biomes. This review demonstrates that ant-bird interactions are a pervasive phenomenon across ecological domains, playing a key role in ecosystem function. Future studies need to combine sensible experimentation within anthropogenic disturbance gradients in order to achieve a better understanding of this interaction.

Grasshoppers do not flee from their alarmed predators but from non-alarmed ones.

Alarm calls produced by basal prey have a well-known informative value. In multi-predator communities, mesopredators, when faced with top predators, may emit alarm calls that could inform basal prey about their lowered predation risk. To test this unexplored possibility, we conducted one field and one mesocosm experiment in which we simulated alarm and non-alarm calls from little owls (Athene noctua) as mesopredators and measured their effects on grasshoppers as prey of little owls but not of top predators. In the field experiment, we found that grasshopper species were significantly more abundant in patches where we simulated either the presence of scared little owls (alarm treatment) or no owls (control treatment) compared to patches where the presence of non-scared little owls (non-alarm treatment) was simulated. In the mesocosm experiment, locusts (Locusta migratoria) moved significantly more to exposed areas when we simulated the presence of scared little owls (alarm treatment) or of a granivorous bird (control treatment), while they moved to sheltered areas when we simulated the presence of non-scared owls (non-alarm treatment). These results show that prey could cue on predators' calls to assess their predation risk and make decisions, revealing unprecedented potential ecological consequences of alarm calls in invertebrate communities.

Geographical variation in pace-of-life in a long-distance migratory bird: implications for population management.

Life-history theory predicts that animals should develop adaptive trade-offs between survival and reproduction to maximize their fitness. This results in a continuum of life-history strategies among species, ranging from slow to fast paces-of-life. The optimal pace-of-life has been shown to vary within environmental gradients, with a commonly observed pattern of a slow-to-fast continuum from the tropics to the poles. Within species, pace-of-life variability has however received much less attention. In this study, we investigated whether or not the pace-of-life of populations within a species follows the expected slow-fast continuum associated with latitude. We analysed the variability of life-history strategies among populations of the European roller Coracias garrulus, a long-distance migratory species, comparing breeding parameters and adult survival between populations across a latitudinal gradient. The findings showed a negative correlation between survival and clutch size in roller populations, with a slower pace-of-life in the northern populations and a faster pace-of-life in the southern populations: a reverse gradient to what might be expected from inter-specific studies. These results suggest that northern populations would benefit from measures enhancing adult survival probability, such as reduction in harvesting rates, while southern populations would respond better to actions favouring reproductive success, such as nesting site provisioning. This study highlights that life-history traits can vary substantially between populations of a single species with a large latitudinal breeding range, and pinpoint how knowledge about this variability may be key in anticipating different populations' responses to threats as well as to conservation strategies.

Avian and rodent responses to the olfactory landscape in a Mediterranean cavity community.

Animals rely on cues informing about future predation risk when selecting habitats to breed in. Olfactory information may play a fundamental role in the assessment of predation threats, because predators produce characteristic body odours, but the role of odours in habitat selection has seldom been considered. Here, we test whether fear of predation induced by odour cues may affect the settlement pattern of a Mediterranean cavity-dependent community of rodents and non-excavator hole-nesting birds. To test this hypothesis, we experimentally manipulated the perception of predation risk on a scale of patch by applying either odours of a carnivore predator (risky odour treatment), lemon essence (non-risky odour treatment) and a control non-odorous treatment and studied bird and rodent settlement patterns. Nest-box occupation probability differed across treatments so that species in the community settled in more numbers in control than in non-risky and than in risky odour-treated nest boxes. Concerning settlement patterns, control nest boxes were occupied more rapidly than nest boxes with odour information. Birds and rodents settled earlier in control than in risky odour-treated nest boxes, but their settlement pattern did not significantly vary between risky odour and non-risky odour-treated nest boxes. Our findings demonstrate that olfactory cues may be used to assess habitat quality by settling species in this community, but we cannot pinpoint the exact mechanism that has given rise to the pattern of preference by nest boxes.

Colour polymorphism in owls is linked to light variability.

Owls show an astonishing variation in their degree of colour polymorphism, although the exact mechanisms driving such variation remain controversial. Here we address this fundamental question by considering information on all extant owls and recent advances in comparative methods in the frame of three mutually non-exclusive evolutionary scenarios. In addition, we study for the first time whether the evolution of influential ecological characters facilitated the evolution of colour polymorphism (or vice versa). In agreement with the niche divergence hypothesis, we found that species living under more variable luminal conditions, i.e., species with diurnal and crepuscular habits and those inhabiting in a mixture of open and closed habitats, were more likely to show colour polymorphism. Correlated evolution analyses revealed that a change in the luminal niche might be a fundamental requisite for the evolution of colour polymorphism. Moreover, polymorphism was more frequent among owl species occupying lower trophic levels, which could be explained by a particularly high selection for crypsis on small predator owls. Our results, thus, provide support for the idea that colour polymorphism in owls is an adaptive character likely maintained by the selective advantage of morphs under different environmental conditions via disruptive selection mechanisms.

Receivers matter: the meaning of alarm calls and competition for nest sites in a bird community.

Animal communities may constitute information networks where individuals gain information on predation risk by eavesdropping on alarm calls of other species. However, communities include species in different trophic levels, and it is not yet known how the trophic level of the receiver influences the informative value of a call. Furthermore, no empirical study has yet tested how increased competition may influence the value of alarm calls for distinct receivers. Here, we identify the importance of alarm calls emitted by a small owl, the little owl (Athene noctua), on the structure of a cavity-nesting bird community including mesopredators and primary prey under variable levels of competition for nest holes. Competitors sharing top predators with the callers and prey of the callers interpreted alarm and non-alarm calls differently. Competitors chose preferentially alarm and non-alarm patches over control patches to breed, while prey selected alarm patches. In contrast, competition for nest sites affected habitat selection of prey species more than that of competitors of the callers. This study provides support for a changing value of alarm calls and competition for nest sites for distinct receivers related to niche overlapping among callers and eavesdroppers, therefore, calling attention to possible cascading effects by the use of information in natural communities.

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.

Evidence of long-term structured cuckoo parasitism on individual magpie hosts.

Brood parasites usually reduce their host's breeding success, resulting in strong selection for the evolution of host defences. Intriguingly, some host individuals/populations show no defence against parasitism, which has been explained within the frame of three different evolutionary hypotheses. One of these hypotheses posits that intermediate levels of defence at the population level may result from nonrandom distribution of parasitism among host individuals (i.e. structured parasitism). Empirical evidence for structured brood parasitism is, however, lacking for hosts of European cuckoos due to the absence of long-term studies. Here, we seek to identify the patterns of structured parasitism by studying great spotted cuckoo parasitism on individual magpie hosts over five breeding seasons. We also aim to identify whether individual characteristics of female magpies and/or their territories were related to the status of repeated parasitism. We found that 28·3% of the females in our population consistently escaped from cuckoo parasitism. Only 11·3% of females were always parasitized, and the remaining 60·4% changed their parasitism status. The percentage of females that maintained their status of parasitism (i.e. either parasitized or nonparasitized) between consecutive years varied over the study. Females that never suffered cuckoo parasitism built bigger nests than parasitized females at the beginning of the breeding season and smaller nests than those of parasitized females later in the season. Nonparasitized females also moved little from year to year and preferred areas with different characteristics over the course of the breeding season than parasitized females. Overall, females escaping from cuckoo parasitism reared twice as many chicks per year than those that were parasitized. In conclusion, our study reveals for first time the existence of a structured pattern of cuckoo parasitism based on phenotypic characteristics of individual hosts and of their territories.

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.

Egg phenotype matching by cuckoos in relation to discrimination by hosts and climatic conditions.

Although parasites and their hosts often coexist in a set of environmentally differentiated populations connected by gene flow, few empirical studies have considered a role of environmental variation in shaping correlations between traits of hosts and parasites. Here, we studied for the first time the association between the frequency of adaptive parasitic common cuckoo Cuculus canorus phenotypes in terms of egg matching and level of defences exhibited by its reed warbler Acrocephalus scirpaceus hosts across seven geographically distant populations in Europe. We also explored the influence of spring climatic conditions experienced by cuckoos and hosts on cuckoo-host egg matching. We found that between-population differences in host defences against cuckoos (i.e. rejection rate) covaried with between-population differences in degree of matching. Between-population differences in host egg phenotype were associated with between-population differences in parasitism rate and spring climatic conditions, but not with host level of defences. Between-population differences in cuckoo egg phenotype covaried with between-population differences in host defences and spring climatic conditions. However, differences in host defences still explained differences in mimicry once differences in climatic conditions were controlled, suggesting that selection exerted by host defences must be strong relative to selection imposed by climatic factors on egg phenotypes.

Sex recognition by odour and variation in the uropygial gland secretion in starlings.

1. Although a growing body of evidence supports that olfaction based on chemical compounds emitted by birds may play a role in individual recognition, the possible role of chemical cues in sexual selection of birds has been only preliminarily studied. 2. We investigated for the first time whether a passerine bird, the spotless starling Sturnus unicolor, was able to discriminate the sex of conspecifics by using olfactory cues and whether the size and secretion composition of the uropygial gland convey information on sex, age and reproductive status in this species. 3. We performed a blind choice experiment during mating, and we found that starlings were able to discriminate the sex of conspecifics by using chemical cues alone. Both male and female starlings preferred male scents. Furthermore, the analysis of the chemical composition of the uropygial gland secretion by using gas chromatography-mass spectrometry (GC-MS) revealed differences between sexes, ages and reproductive status. 4. In conclusion, our study reveals for first time that a passerine species can discriminate the sex of conspecifics by relying on chemical cues and suggests that the uropygial gland secretion may potentially function as a chemical signal used in mate choice and/or intrasexual competition in this species.

Predation risk determines breeding territory choice in a Mediterranean cavity-nesting bird community.

Non-direct effects of predation can be an important component of the total effect of predation, modulating animal population and community dynamics. The isolated effects of predation risk on the spatial organisation of the breeding bird community, however, remains poorly studied. We investigated whether an experimentally increased predation risk prior to reproduction affected breeding territory selection and subsequent reproductive strategies in three Mediterranean cavity-nesting birds, i.e., the little owl Athene noctua, European roller Coracias garrulus and scops owl Otus scops. We found that territories used the previous year were more likely to be re-occupied when they belonged to the safe treatment rather than to the risky treatment. The first choice of breeders of all three species was for safe territories over risky ones. When all breeding attempts in the season (i.e., final occupation) were considered, breeders also preferred safe to risky sites. In addition, little owls laid larger eggs in risky territories than in safe territories. Our study provides experimental evidence of a rapid preventive response of the three most abundant species in a cavity-nesting bird community to a short-term manipulation of predation risk. This response highlights the key role of the non-direct effects of predation in modulating avian community organisation.

Visual cues and parental favouritism in a nocturnal bird.

Visual signals are crucial for parent-offspring communication, although their functioning has been neglected for nocturnal birds. Here, we investigated parental preference for nestling coloration in nocturnal conditions--a question hitherto unexplored--in a nocturnal raptor, the scops owl (Otus scops). We assessed how parents allocated food during the night in relation to a manipulation of ultraviolet (UV) reflectance of the cere (skin above the beak) of their offspring. Reflectance of the cere shows a marked peak in the UV part of the spectrum, and location of the UV peak is related to nestling body mass (i.e. heavier nestlings have a UV peak at lower wavelengths). We found evidence of parental bias in favour of lighter offspring: UV-reduced nestlings gained more weight during the night than their control siblings. This study provides the first experimental evidence of the use of visual cues for parent-offspring communication in a nocturnal bird.

Do spotless starlings place feathers at their nests by ultraviolet color?

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.

Avian egg and nestling detection in the wild: should we rely on visual models or behavioural experiments?

The fields of avian egg and nestling colour detection have rapidly advanced owing to the application of visual models, which have allowed assessing of evolutionary questions considering receiver perception. Here, I first review the literature aiming to identify patterns of avian visual model usage. Second, I elaborate on limitations in the application of the receptor-noise limited perceptual (RNL hereafter) model. A systematic literature review revealed that the RNL model was the most used approach (81% of studies) in the field, and that most studies (76%) were concerned with classic evolutionary questions in avian brood parasitism. Some known limitations of the RNL model deal with model assumptions and parameterization, or, a poor consideration of post-detection neural processes. Others, however, are specific of the fields of egg and nestling discrimination and deal with the highly variable nature of ambient light at the nests, the complex colour design of eggs and nestlings, the multi-dimensional nature of perception, and the possible implication of learning. I, therefore, conclude that visual models should be used with caution to establish inference about egg and nestling discrimination, and rather be used to provide reasonable hypotheses which need to be validated with behavioural experiments. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

Melanism influences the use of social information in a polymorphic owl.

Social information use has well-known fitness benefits. However, causes underlying the apparent inter-individual variability in the propensity to use social information are poorly studied. Melanins are pigments responsible for most of intra-specific color variation in vertebrates and their variation is often associated with changes in behaviour. Here, we explored whether melanism is related to individual propensity to use social information in the color polymorphic scops owl Otus scops. We manipulated social information on predation risk at nests by broadcasting calls of the sympatric little owl Athene noctua and found that owlets of brownish females exposed to alarm calls had lower levels of natural antibodies than those of greyish females. In parallel, we found changes in parental behaviour contingent on coloration because when exposed to the risky treatment brownish females returned earlier to nests than greyish females and owlets raised by brownish females were fed with smaller prey than those raised by greyish ones. These results provide support for a previous ignored role of melanins on the propensity to use social information, which may help to explain the maintenance of melanin-based color polymorphisms wherever social environments are variable.

Phaeomelanin matters: Redness associates with inter-individual differences in behaviour and feather corticosterone in male scops owls (Otus scops).

Individuals within populations often show consistent variation in behavioural and physiological traits which are frequently inter-correlated, potentially leading to phenotypic integration. Understanding the mechanisms behind such integration is a key task in evolutionary ecology, and melanin based colouration has been suggested to play a pivotal role. In birds, most of plumage colour variation is determined by two types of melanin, eumelanin and phaeomelanin, but the role of phaeomelanin in avian phenotype integration has been barely investigated. Here, we test for covariation between phaeomelanin-based colouration, behavioural traits (i.e. nest territoriality, aggressiveness, breath rate and parental behaviour) and corticosterone in feathers in the polymorphic scops owl Otus scops, a bird species in which more phaeomelanic individuals display reddish colourations. In males, we observed that reddish males took longer to return to their nests and showed higher levels of feather CORT than more greyish ones. Behaviour and feather CORT were not associated to plumage colour in females. The found associations between redness, behaviour and feather CORT in males, but not in females, might suggest the existence of a sex-specific integrated phaeomelanic phenotype in scops owls.

Dark nests and conspicuousness in color patterns of nestlings of altricial birds.

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.

Sexually selected egg coloration in spotless starlings.

It has been recently proposed that the blue-green coloration in eggs of many avian species may constitute a sexually selected female signal. Blue-green color intensity would reflect the physiological condition of females, and hence it might also affect the allocation of male parental care. In this study, we use three different experimental approaches to explore the importance of sexual selection on blue-green egg coloration of spotless starling (Sturnus unicolor) eggs. First, experimental deterioration of female body condition (by means of wing feather removal) negatively affected the intensity of blue-green egg coloration. Second, blue-green color intensity of artificial model eggs had a significant positive influence on paternal feeding effort. Finally, we found a negative relationship between the effect of experimental food supply on nestling immunocompetence and the intensity of blue-green coloration of eggs, suggesting that egg color predicts nutritional conditions that nestlings will experience during development. All these results taken together strongly support a role of sexual selection in the blue-green coloration of spotless starling eggs.

Egg colour mimicry in the common cuckoo Cuculus canorus as revealed by modelling host retinal function.

Some parasite cuckoo species lay eggs that, to the human eye, appear to mimic the appearance of the eggs of their favourite hosts, which hinders discrimination and removal of their eggs by host species. Hitherto, perception of cuckoo-host egg mimicry has been estimated based on human vision or spectrophotometry, which does not account for what the receivers' eye (i.e. hosts) actually discriminates. Using a discrimination model approach that reproduces host retinal functioning, and museum egg collections collected in the south of Finland, where at least six different races of the European cuckoo (Cuculus canorus) coexist, I first assess whether the colour design of cuckoo eggs of different races maximizes matching for two favourite avian hosts, viz. the redstart (Phoenicurus phoenicurus) and the pied wagtail (Motacilla alba). Second, I assess the role of nest luminosity on host perception of mimicry by the same two hosts. Phoenicurus-cuckoo eggs showed a better chromatic matching with the redstart-host eggs than other cuckoo races, and in most cases can not be discriminated. Sylvia-cuckoo eggs, however, showed better achromatic matching with redstart-host eggs than Phoenicurus-cuckoo eggs. Also, Motacilla-cuckoo eggs showed poorer chromatic and achromatic matching with pied wagtail-host eggs than Sylvia-cuckoo eggs. Nest luminosity affected chromatic and achromatic differences between cuckoo and host eggs, although only minimally affected the proportion of cuckoo eggs discriminated by chromatic signals. These results reveal that cuckoo races as assessed by humans do not entirely match with host perception of matching and that achromatic mechanisms could play a main role in the discrimination of cuckoo eggs at low-light levels.