Egg cooling associated with nest size in a passerine bird.

Breeders evolved adaptive responses to rapid changes in ambient temperature. In birds, nests are expected to reduce egg cooling when the incubator is temporarily off the eggs. Here we present the results of two complementary laboratory experiments aiming at testing the association between egg cooling and the thickness of the nest under and surrounding the eggs in a non-domesticated avian model species (great tit, Parus major). To simulate incubation behaviour, we exposed nests with 4-egg clutches to a heat source until the eggs reached a normal incubation temperature (ca. 39 °C) and then recorded egg cooling 8 min after removal of the heat source, which corresponds to the time females generally leave eggs unattended during the incubation period. Eggs cooled more quickly when the nest layer under the eggs was thinner and when ambient temperature was cooler. We also show that the wall around the nest cup is important to buffer egg cooling. It is hypothesised that in bird nests, both the thickness of the material under the eggs, and the wall surrounding the nest cup interact to maintain a heat envelope around the eggs for the time the incubating parent is foraging. This could explain why the thickness of the nest base and wall are adjusted to the ambient temperature the birds experience during the nest building phase, to anticipate the thermal conditions during incubation and preserve egg viability.

Surface temperatures of non-incubated eggs in great tits (Parus major) are strongly associated with ambient temperature.

Temperature is one of the best investigated environmental factors in ecological life-history studies and is increasingly considered in the contexts of climate change and urbanization. In avian ecology, few studies have examined the associations between thermal dynamics in the nest environment and its neighbouring air. Here, we placed avian nests and non-incubated eggs inside nest boxes at various air temperatures that ranged from 0.3 to 33.1 °C, both in the field and in laboratory conditions. We measured how the design of the boxes, their compass orientation and their location in more or less urbanized environments affected the surface temperature of nests and eggs. We also assessed whether covering the eggs with lining material influenced their surface temperature. Overall, across all performed tests, we found that the surface temperature of nests and eggs strongly reflected the air temperature measured outside of the nest boxes. While the design of the nest boxes had little influence on the temperature of nests and eggs, orienting the nest boxes to the north or to the west significantly decreased their surface temperature. The presence of lining material also kept eggs slightly warmer when air temperatures were low. Altogether these results suggest that non-incubated eggs are not well protected against extreme air temperatures prior to the onset of incubation. From an evolutionary point of view, producers of ectotherm eggs need therefore to time egg-laying appropriately in order to avoid unfavourable thermal nest environments.

Effects of interspecific coexistence on laying date and clutch size in two closely related species of hole-nesting birds.

Coexistence between great tits Parus major and blue tits Cyanistes caeruleus, but also other hole-nesting taxa, constitutes a classic example of species co-occurrence resulting in potential interference and exploitation competition for food and for breeding and roosting sites. However, the spatial and temporal variations in coexistence and its consequences for competition remain poorly understood. We used an extensive database on reproduction in nest boxes by great and blue tits based on 87 study plots across Europe and Northern Africa during 1957-2012 for a total of 19,075 great tit and 16,729 blue tit clutches to assess correlative evidence for a relationship between laying date and clutch size, respectively, and density consistent with effects of intraspecific and interspecific competition. In an initial set of analyses, we statistically controlled for a suite of site-specific variables. We found evidence for an effect of intraspecific competition on blue tit laying date (later laying at higher density) and clutch size (smaller clutch size at higher density), but no evidence of significant effects of intraspecific competition in great tits, nor effects of interspecific competition for either species. To further control for site-specific variation caused by a range of potentially confounding variables, we compared means and variances in laying date and clutch size of great and blue tits among three categories of difference in density between the two species. We exploited the fact that means and variances are generally positively correlated. If interspecific competition occurs, we predicted a reduction in mean and an increase in variance in clutch size in great tit and blue tit when density of heterospecifics is higher than the density of conspecifics, and for intraspecific competition, this reduction would occur when density of conspecifics is higher than the density of heterospecifics. Such comparisons of temporal patterns of means and variances revealed evidence, for both species, consistent with intraspecific competition and to a smaller extent with interspecific competition. These findings suggest that competition associated with reproductive behaviour between blue and great tits is widespread, but also varies across large spatial and temporal scales.

Disentangling drivers of reproductive performance in urban great tits: a food supplementation experiment.

Worldwide urban expansion induces degradation of the natural environment, resulting in new constraints in terms of breeding sites, anthropogenic disturbances as well as food resources. The alteration of resource abundance and type may induce non-adaptive investments in reproduction from urban dwellers. Food availability and quality have been identified as potential drivers of the decline in passerine body mass and fledging success in urbanized landscapes, particularly if birds misinterpret cues of food abundance used to adjust their reproductive investment. In a previous study, we demonstrated in urban great tits, Parus major, that highly preferred larger cavities have larger clutches with lower breeding success, leading to a maladaptive breeding investment. Previous studies also showed that urban great tits are smaller or thinner than rural ones, both at nestling and adult stages. Here, we present the results of a food-supplementation experiment to examine whether food resources mediate this maladaptive breeding investment and constrain the reproductive performance of this urban bird population. We predicted higher performance in food-supplemented broods, especially in larger cavities, and stronger effects of the supplementation in more artificialized territories. Surprisingly, we found that food-supplemented nestlings and their parents had lower body mass and condition, especially in areas with more pedestrians. Supplementation was also associated with lower nestling survival until fledging in places that presented lower levels of naturalness, independently of cavity size. This work highlights a lack of knowledge on avian feeding behaviour in cities, a key element for understanding how breeding performance is affected by human presence and habitat naturalness.

Nest design in a changing world: great tit Parus major nests from a Mediterranean city environment as a case study.

Investigations of urbanization effects on birds have focused mainly on breeding traits expressed after the nest-building stage (e.g. first-egg date, clutch size, breeding success, and offspring characteristics). Urban studies largely ignored how and why the aspects of nest building might be associated with the degree of urbanization. As urban environments are expected to present novel environmental changes relative to rural environments, it is important to evaluate how nest-building behavior is impacted by vegetation modifications associated with urbanization. To examine nest design in a Mediterranean city environment, we allowed urban great tits (Parus major) to breed in nest boxes in areas that differed in local vegetation cover. We found that different measures of nest size or mass were not associated with vegetation cover. In particular, nests located adjacent to streets with lower vegetation cover were not smaller or lighter than nests in parks with higher vegetation cover. Nests adjacent to streets contained more pine needles than nests in parks. In addition, in nests adjacent to streets, nests from boxes attached to pine trees contained more pine needles than nests from boxes attached to other trees. We suggest that urban-related alterations in vegetation cover do not directly impose physical limits on nest size in species that are opportunistic in the selection of nesting material. However, nest composition as reflected in the use of pine needles was clearly affected by habitat type and the planted tree species present, which implies that rapid habitat change impacts nest composition. We do not exclude that urbanization might impact other aspects of nest building behaviour not covered in our study (e.g. costs of searching for nest material), and that the strengths of the associations between urbanization and nest structures might differ among study populations or species.

Female blue tits with brighter yellow chests transfer more carotenoids to their eggs after an immune challenge.

Female ornaments are present in many species, and it is more and more accepted that sexual or social selection may lead to their evolution. By contrast, the information conveyed by female ornaments is less well understood. Here, we investigated the links between female ornaments and maternal effects. In birds, an important maternal effect is the transmission of resources, such as carotenoids, into egg yolk. Carotenoids are pigments with antioxidant and immunomodulatory properties that are crucial for females and developing offspring. In blue tits, we evaluated whether ultraviolet (UV)/blue and yellow feather colouration signals a female's capacity to allocate carotenoids to egg yolk. Because mounting an immune response is costly and trade-offs are more detectable under harsh conditions, we challenged the immune system of females before laying and examined the carotenoid level of their eggs afterward. A positive association between feather carotenoid chroma and egg carotenoid level would be expected if yellow colouration signals basal immunity. Alternatively, if female colouration more generally reflects maternal capacity to invest in reproduction under challenging conditions, then other components of colouration (i.e. yellow brightness and UV/blue colouration) could be linked to maternal capacity to invest in eggs. No association between egg carotenoid levels and UV/blue crown colouration or female yellow chest chroma was found; the latter result suggests that yellow colouration does not signal immune capacity at laying in this species. By contrast, we found that, among females that mounted a detectable response to the vaccine, those with brighter yellow chests transmitted more carotenoids into their eggs. This result suggests yellow brightness signals maternal capacity to invest in reproduction under challenging conditions, and that male blue tits may benefit directly from choosing brighter yellow females.

Aromatic plants in nests of the blue tit Cyanistes caeruleus protect chicks from bacteria.

Several bird species add fresh fragments of plants which are rich in volatile secondary compounds to their nests. It has been suggested, although never tested, that birds use fresh plants to limit the growth of nest microorganisms. On Corsica, blue tits (Cyanistes caeruleus) incorporate fresh fragments of aromatic plants into their nests. These plants do not reduce infestation by nest ectoparasites, but have been shown to improve growth and condition of chicks at fledging. To understand the mechanisms underlying such benefits, we experimentally tested the effects of these plants on the bacteria living on blue tits. Aromatic plants significantly affected the structure of bacterial communities, in particular reducing bacterial richness on nestlings. In addition, in this population where there is a strong association between bacterial density and infestation by blood-sucking Protocalliphora blow fly larvae, these plants reduced bacterial density on the most infested chicks. Aromatic plants had no significant effect on the bacteria living on adult blue tits. This study provides the first evidence that fresh plants brought to the nests by adult birds limit bacterial richness and density on their chicks.

Interspecific variation in the relationship between clutch size, laying date and intensity of urbanization in four species of hole-nesting birds.

The increase in size of human populations in urban and agricultural areas has resulted in considerable habitat conversion globally. Such anthropogenic areas have specific environmental characteristics, which influence the physiology, life history, and population dynamics of plants and animals. For example, the date of bud burst is advanced in urban compared to nearby natural areas. In some birds, breeding success is determined by synchrony between timing of breeding and peak food abundance. Pertinently, caterpillars are an important food source for the nestlings of many bird species, and their abundance is influenced by environmental factors such as temperature and date of bud burst. Higher temperatures and advanced date of bud burst in urban areas could advance peak caterpillar abundance and thus affect breeding phenology of birds. In order to test whether laying date advance and clutch sizes decrease with the intensity of urbanization, we analyzed the timing of breeding and clutch size in relation to intensity of urbanization as a measure of human impact in 199 nest box plots across Europe, North Africa, and the Middle East (i.e., the Western Palearctic) for four species of hole-nesters: blue tits (Cyanistes caeruleus), great tits (Parus major), collared flycatchers (Ficedula albicollis), and pied flycatchers (Ficedula hypoleuca). Meanwhile, we estimated the intensity of urbanization as the density of buildings surrounding study plots measured on orthophotographs. For the four study species, the intensity of urbanization was not correlated with laying date. Clutch size in blue and great tits does not seem affected by the intensity of urbanization, while in collared and pied flycatchers it decreased with increasing intensity of urbanization. This is the first large-scale study showing a species-specific major correlation between intensity of urbanization and the ecology of breeding. The underlying mechanisms for the relationships between life history and urbanization remain to be determined. We propose that effects of food abundance or quality, temperature, noise, pollution, or disturbance by humans may on their own or in combination affect laying date and/or clutch size.

Early seasonal development of brain song control nuclei in male blue tits.

In songbirds, the seasonal growth of the song system is generally thought to be controlled by the spring increase in plasma levels of testosterone and/or related changes in singing activity. Here we report an extremely early seasonal growth (before February) of the song control nuclei HVC and RA in Corsican blue tits (Parus caeruleus) indicating that the vernal development of these nuclei occurs well before the vernal increase in plasma testosterone, testes size and song activity. The development of HVC and RA occurred simultaneously in two populations that are known to breed consistently 1 month apart as an adaptation to heterogeneous landscapes (predominance of broad-leaved deciduous versus evergreen oak trees). The unidentified environmental and/or physiological cues controlling the plasticity in the song system must therefore differ, at least in part, from those affecting other morphological and physiological traits controlling reproduction.

Parasitism reduces the potential for evolution in a wild bird population.

We tested the effect of detrimental environmental conditions during growth on the heritability of chick body size in a wild population of blue tits (Parus caeruleus) highly parasitized by blowfly larvae. During nine years, we experimentally induced deparasitized broods, whereas unmanipulated control broods remained heavily infested by two species of Protocalliphora ectoparasites. The heritability of tarsus length was significantly higher in deparasitized broods than control broods, due in part to a very low common brood environment effect in deparasitized broods. We also found evidence for significant genotype-by-environment interactions, which further reflected the effect of the ecological conditions on the expression of additive genetic effects and could represent an additional constraint on the evolution of tarsus length. To our knowledge, this experiment provides the first evidence of host quantitative genetics being influenced by parasitism, and illustrates the potential for parasitism to constrain an evolutionary response to selection.

Climate variation and regional gradients in population dynamics of two hole-nesting passerines.

Latitudinal gradients in population dynamics can arise through regional variation in the deterministic components of the population dynamics and the stochastic factors. Here, we demonstrate an increase with latitude in the contribution of a large-scale climate pattern, the North Atlantic Oscillation (NAO), to the fluctuations in size of populations of two European hole-nesting passerine species. However, this influence of climate induced different latitudinal gradients in the population dynamics of the two species. In the great tit the proportion of the variability in the population fluctuations explained by the NAO increased with latitude, showing a larger impact of climate on the population fluctuations of this species at higher latitudes. In contrast, no latitudinal gradient was found in the relative contribution of climate to the variability of the pied flycatcher populations because the total environmental stochasticity increased with latitude. This shows that the population ecological consequences of an expected climate change will depend on how climate affects the environmental stochasticity in the population process. In both species, the effects will be larger in those parts of Europe where large changes in climate are expected.

Is the small clutch size of a Corsican blue tit population optimal?

In an attempt to test predictions of the optimisation hypothesis of life history traits in birds, we estimated fitness consequences of brood size manipulations. Experiments were carried out over a period of 4 years in a Mediterranean population of blue tits Parus caeruleus which is confronted with a particular set of environmental constraints. Effects of brood size manipulation were investigated in relation to year-to-year variation in environmental conditions, especially caterpillar abundance. There was a strong variation in the effects of brood size manipulation depending on year. Most effects were on offspring quality (fledging mass, tarsus length). The absolute number of recruits did not significantly differ among categories (reduced, control, enlarged broods) but varied considerably among years. Females recruited from enlarged broods were of lower quality, started to breed later and laid fewer eggs than those recruited from control and reduced broods. Neither parental survival nor reproductive performances of adults in year n + 1 was affected by brood size manipulation in year n. Thus there was no evidence for a cost of reproduction in this population. Since the number of recruits did not depend on brood size manipulation (recruitment rates were higher in reduced broods), but recruits from reduced broods were of better quality compared with other groups, we conclude that adults lay a clutch that is larger than that which is predicted by the optimisation hypothesis. Producing more young could incur some penalties because offspring from large broods are of lower quality and less likely to recruit in the population. Two possible reasons why decision rules in this population seem to be suboptimal are discussed.

Physiological ecology of Mediterranean blue tits (Parus caeruleus L.): effects of ectoparasites (Protocalliphora spp.) and food abundance on metabolic capacity of nestlings.

The consequences of nest ectoparasites, such as Protocalliphora larvae, on nestling birds have been the subject of numerous studies. Despite observed reductions in mass and hematocrit of chicks from parasitized nests, no studies have found any effect of Protocalliphora on nestling survival, suggesting that fitness consequences of Protocalliphora are either weak or occur after fledging. From experiments on the metabolic performance of chicks, we found that parasitized chicks suffer from reduced thermogenic and metabolic capacities as a result of decreased mass and hematocrit. Hence, Protocalliphora may potentially affect nestling survival after fledging, when energetically costly activities such as flight and moult are undertaken. Previous studies have demonstrated an increase in parental feeding rate to compensate for the detrimental consequences of parasite infestation. We tested whether parasite effects on nestling aerobic capacity were dependent on food availability during the feeding period. Measures of caterpillar densities and experimental manipulations of parasite loads allowed us to investigate relationships among host, parasite, and environment. A positive relationship between chick aerobic and thermogenic performances and caterpillar density suggests that negative effects of parasitism may be offset by increased food availability. This study provides the first measurement of the effects of an ectoparasite on metabolic competence in wild birds and documentation of the effect of food availability on ectoparasite virulence using a quantitative measure of food abundance.

The design and function of birds' nests.

All birds construct nests in which to lay eggs and/or raise offspring. Traditionally, it was thought that natural selection and the requirement to minimize the risk of predation determined the design of completed nests. However, it is becoming increasingly apparent that sexual selection also influences nest design. This is an important development as while species such as bowerbirds build structures that are extended phenotypic signals whose sole purpose is to attract a mate, nests contain eggs and/or offspring, thereby suggesting a direct trade-off between the conflicting requirements of natural and sexual selection. Nest design also varies adaptively in order to both minimize the detrimental effects of parasites and to create a suitable microclimate for parents and developing offspring in relation to predictable variation in environmental conditions. Our understanding of the design and function of birds' nests has increased considerably in recent years, and the evidence suggests that nests have four nonmutually exclusive functions. Consequently, we conclude that the design of birds' nests is far more sophisticated than previously realized and that nests are multifunctional structures that have important fitness consequences for the builder/s.

Local individual preferences for nest materials in a passerine bird.

BACKGROUND: Variation in the behavioural repertoire of animals is acquired by learning in a range of animal species. In nest-building birds, the assemblage of nest materials in an appropriate structure is often typical of a bird genus or species. Yet plasticity in the selection of nest materials may be beneficial because the nature and abundance of nest materials vary across habitats. Such plasticity can be learned, either individually or socially. In Corsican populations of blue tits Cyanistes caeruleus, females regularly add in their nests fragments of several species of aromatic plants during the whole breeding period. The selected plants represent a small fraction of the species present in the environment and have positive effects on nestlings. METHODOLOGY/PRINCIPAL FINDINGS: We investigated spatiotemporal variations of this behaviour to test whether the aromatic plant species composition in nests depends on 1) plant availability in territories, 2) female experience or 3) female identity. Our results indicate that territory plays a very marginal role in the aromatic plant species composition of nests. Female experience is not related to a change in nest plant composition. Actually, this composition clearly depends on female identity, i.e. results from individual preferences which, furthermore, are repeatable both within and across years. A puzzling fact is the strong difference in plant species composition of nests across distinct study plots. CONCLUSIONS/SIGNIFICANCE: This study demonstrates that plant species composition of nests results from individual preferences that are homogeneous within study plots. We propose several hypotheses to interpret this pattern of spatial variation before discussing them in the light of preliminary results. As a conclusion, we cannot exclude the possibility of social transmission of individual preferences for aromatic plants. This is an exciting perspective for further work in birds, where nest construction behaviour has classically been considered as a stereotypic behaviour.

Circulating corticosterone levels in breeding blue tits Parus caeruleus differ between island and mainland populations and between habitats.

Little is known about whether adaptations to an insular life also involve adaptations in basal corticosterone levels or in the adrenocortical stress response, thus being part of a genetically based island syndrome. However, differences in corticosterone between island and mainland may also be a direct phenotypic response to differences in environmental conditions or may depend on individual characteristics of the animal such as body condition or parental investment. In this paper, we investigated whether insular (Island of Corsica) and mainland (nearby Southern France) blue tits Parus caeruleus populations differed in baseline and handling-stress induced corticosterone levels during the breeding season as a response to biological changes of insular biota. We also examined whether corticosterone levels of both mainland and insular blue tits differed between birds living in two different habitats (summergreen and evergreen oak woods) that differ in food availability and whether individual characteristics affected corticosterone levels. We found (a) differences in baseline corticosterone plasma levels between Corsica and the mainland, independent of regional differences in fat scores, (b) a regional difference in the relationship between corticosterone levels and brood size, (c) a difference in the rapidity of onset of the stress response to handling between habitats, independent of region, and (d) a negative relationship between body fat stores and baseline corticosterone levels independent of region. Reduced baseline corticosterone levels on Corsica may be a component of the insular syndrome, allowing birds to be less aggressive and to enhance parental investment despite higher breeding densities. We suggest that baseline corticosterone levels are only elevated if food availability affects directly the parents. However, when conditions deteriorate unexpectedly (as mimicked by handling stress), food allocation between parents and offspring needs to be re-adjusted in favor of the parents, possibly by increased circulating corticosterone levels. The switch to self-maintenance seems to be modified by the amount of body energy stores.

Endocrine correlates of the breeding asynchrony between two Corsican populations of blue tits (Parus caeruleus).

Analyses of the development of the reproductive system in seasonally breeding birds in the framework of long-term ecological studies are rare. Here, we present the first results of such a study in two Corsican populations of a European passerine bird, the blue tit (Parus caeruleus). The two study populations occupy different oak habitats and are separated by only 25 km. Despite their close proximity, they show a one-month difference in onset of egg laying, even after controlling for altitude. This micro-geographic difference in breeding date appears adaptive because both study populations raise chicks when food is most plentiful. In our study, males reached their maximum song activity during the egg-laying stage while maximal testosterone levels and testes sizes were reached 2-3 weeks before egg laying. The rate of development of the reproductive system in males was much faster in the earlier population, in spite of a similar onset of gonad development and song activity for the two study populations. No change in the volume of the song-control nuclei (HVC and RA) could be detected during the study period. Development of brain nuclei was completed 2-3 months before the beginning of intense sexual activity.

Aromatic plants in bird nests as a protection against blood-sucking flying insects?

The nest protection hypothesis suggests that some of the fresh plant material, brought by some bird species to their nests, contain secondary compounds that repel parasites or mask the chemical cues that parasites use to find the host. Corsican blue tits (Parus caeruleus) bring pieces of several species of aromatic plants to the nest at dusk, suggesting a protection against nocturnal agents such as blood-sucking flying insects. The potential repellent or masking effect of these aromatic plant species, alone or in mixture, was experimentally investigated in the mosquito Culex pipiens, using domestic chicks as bird hosts. Aromatic plants had a repellent effect against mosquitoes, although a masking effect could not be ruled out. The plant mixture was the most efficient, although some aromatic plants had a significant effect when used individually. These results are discussed in the context of the nest-protection hypothesis and of the impact of flying blood-sucking insects on bird behaviour and life history traits.

Habitat quality as a predictor of spatial variation in blue tit reproductive performance: a multi-plot analysis in a heterogeneous landscape.

Vertebrate studies have rarely investigated the influence of spatial variation in habitat richness on both short-term (breeding) and long-term (offspring recruitment) reproductive performance using simultaneously multi-patch, multi-habitat type and multi-year approaches at landscape level. Here we present results of such an approach using the influence of two oak tree (Quercus ilex, Q. humilis) species on reproductive performance in Corsican blue tits (Parus caeruleus ogliastrae) as a model system. We found that blue tits breeding in rich broad-leaved deciduous patches consistently laid eggs earlier in the season, and produced larger clutches and more fledglings of higher quality, than those breeding in poor evergreen patches. Also, parents, especially males, were in better physical condition in the broad-leaved deciduous than in the evergreen patches. Surprisingly, estimates of long-term effects of reproduction, such as recruitment rates of locally born offspring, did not differ between the two habitat types. Our results suggest that short-term breeding performance and phenotypic quality of both chicks and parents do not necessarily provide reliable information about contributions to following generations at a scale larger than that of the local study plot. Differences in reproductive performance between the two oak habitat types could not be attributed to density-dependent effects, differences in levels of nest predation, or differences in age structure of the birds. We suggest that habitats that are optimal for breeding are not necessarily optimal for survival after the breeding season.