Individual Variation in Sleep-Wake Rhythms in Free-Living Birds

Ultradian rhythms, such as sleep-wake periodicities, during the night might represent basic rest-activity cycles of organisms that are fundamental to the temporal organization and synchronization of behavior throughout the day. However, in contrast to circadian rhythms, little is known about the underlying oscillators and molecular mechanisms of higher-frequency rhythms. A fundamental step for the understanding of the mechanisms of these latter periodicities is the analysis of variation in sleep-wake cycles in free-living animals, which can help in estimating the relative importance of genetic and environmental influence on the rhythmicity. We analyzed variation in the level of rhythmicity and period length (τ) of behaviorally defined sleep-wake cycles in a natural population of blue tits Cyanistes caeruleus. Our results indicate that the expression of periodicity in sleep-wake patterns, but not τ, has a strong individual-specific basis. The within-individual repeatability estimate of the expression of periodicity was .45 (95% confidence interval: .35–.55) when data from males and females were combined. In addition, periodicity was influenced by specific environmental factors, such as night temperature, seasonal date, and age of the individual. Most strikingly, low nighttime temperature negatively affected periodicity of sleep-wake patterns, potentially via a hypothermic response of the birds. Our results further suggest that τ is influenced by photoperiod. Blue tits showed longer sleep-wake rhythms when the nights were longer. These observations suggest a genetic basis for the incidence of rhythmic sleep-wake behavior in addition to environmental modifications of their specific expression. (Author correspondence: mueller@orn.mpg.de)     

What do we really know about the signalling role of plumage colour in blue tits? A case study of impediments to progress in evolutionary biology

Evolutionary biologists seek to explain the origin and maintenance of phenotypes, and a substantial portion of this research is accomplished by thorough study of individual species. For instance, many researchers study individual species to understand evolution of ornamental traits which appear to be products of sexual selection. I explored our understanding of sexual ornaments in a well‐studied vertebrate species that may serve as a case study for research programs in evolutionary biology. I attempted to located all published papers examining plumage colour and variables related to sexual selection hypotheses in a common European songbird, the blue tit (Cyanistes caeruleus). Researchers have estimated over 1200 statistical relationships with plumage colour of blue tits in 52 studies. However, of the approximately 1000 main‐effect relationships from the 48 studies that are candidates for inclusion in this meta‐analysis, more than 400 were reported without details of strength and direction. Circumstantial evidence suggests that an unknown number of other estimated effects remain unpublished. Missing information is a substantial barrier to interpretation of these papers and to meta‐analytic synthesis. Examination and analysis of funnel plots indicated that unpublished effects may be a biased sample of all effects, especially for comparisons of plumage colour to age and individual quality, and possibly also to measures of mate choice. Further, type I error was likely elevated by the large number of statistical comparisons evaluated, the frequent use of iterative model‐building procedures, and a willingness to interpret a wide variety of results as support for a hypothesis. Type I errors were made more problematic because blue tit plumage researchers only rarely have attempted to replicate important findings in their own work or that of others. Replication is essential to drawing robust scientific conclusions, especially in probabilistic systems with moderate to weak effects or a likelihood of bias. Last, researchers studying blue tit plumage have often developed ad hoc explanations for deviations of results from their predictions. Revising hypotheses in light of data is appropriate, but these revised hypotheses were rarely tested with new data. The only highly robust conclusion supported by meta‐analysis is that male blue tits have plumage that reflects more light in the ultraviolet and yellow wavelengths than the plumage of females. Various other effects, including condition‐dependence of plumage colour expression and a tendency for females to adjust the sex ratio of their offspring in response to male colour, remain uncertain. These obstacles to progress in the blue tit plumage literature are likely common in evolutionary biology, and so I recommend changes to incentive structures which may improve progress towards scientific understanding in this discipline.     

Fecundity selection on ornamental plumage colour differs between ages and sexes and varies over small spatial scales

Avian plumage colours are some of the most conspicuous sexual ornaments, and yet standardized selection gradients for plumage colour have rarely been quantified. We examined patterns of fecundity selection on plumage colour in blue tits (Cyanistes caeruleus L.). When not accounting for environmental heterogeneity, we detected relatively few cases of selection. We found significant disruptive selection on adult male crown colour and yearling female chest colour and marginally nonsignificant positive linear selection on adult female crown colour. We discovered no new significant selection gradients with canonical rotation of the matrix of nonlinear selection. Next, using a long-term data set, we identified territory-level environmental variables that predicted fecundity to determine whether these variables influenced patterns of plumage selection. The first of these variables, the density of oaks within 50 m of the nest, influenced selection gradients only for yearling males. The second variable, an inverse function of nesting density, interacted with a subset of plumage selection gradients for yearling males and adult females, although the strength and direction of selection did not vary predictably with population density across these analyses. Overall, fecundity selection on plumage colour in blue tits appeared rare and inconsistent among sexes and age classes.     

Corticosterone metabolites in blue tit and pied flycatcher droppings: effects of brood size, ectoparasites and temperature

The hypothalamic-pituitary-adrenal (HPA) axis of birds induces the secretion of corticosterone (CORT) as a response to different ecological variables. In this study we tested experimentally if manipulations of brood size or ectoparasitism led to subsequent differences in the concentration of excreted CORT metabolites of adult and nestling blue tits (Cyanistes caeruleus). No significant effect of the manipulation of brood size was detected in adults or nestlings. No significant effect of ectoparasitism was detected in males or nestlings, although females from uninfested nests showed lower concentrations of excreted CORT metabolites. In addition, we analysed if weather conditions had an influence on the concentration of excreted CORT metabolites of blue tits and pied flycatchers (Ficedula hypoleuca) breeding in the same forest. We detected no effect of weather conditions on adults, but nestlings of both species showed a negative correlation between their excreted CORT metabolites and the average mean temperatures they were subjected to during their growth. This effect was not found in blue tits in a colder year, suggesting that the sensitivity of the HPA axis to ambient temperature may be subjected to interannual variation. Moreover, we found a positive effect of the maximum temperature on the day of sampling on the concentration of CORT metabolites of blue tit nestlings in one of the years. These results suggest that weather conditions may act as environmental stressors to which the HPA axis of blue tit and pied flycatcher nestlings may be sensitive.     

Condition-dependent genetic benefits of extrapair fertilization in female blue tits Cyanistes caeruleus

In many socially monogamous birds, both partners perform extrapair copulations (EPC). As this behaviour potentially inflicts direct costs on females, they are currently hypothesized to search for genetic benefits for descendants, either as 'good' or 'complementary' genes. Although these hypotheses have found some support, several studies failed to find any beneficial consequence of EPC, and whether this behaviour is adaptive to females is subject to discussion. Here, we test these two hypotheses in a natural population of blue tits by accounting for the effect of most parameters known to potentially affect extrapair fertilization. Results suggest that female body mass affected the type of extrapair genetic benefits obtained. Heavy females obtained extrapair fertilizations when their social male was of low quality (as reflected by sexual display) and produced larger extrapair than within-pair chicks. Lean females obtained extrapair fertilizations when their social mate was genetically similar, thereby producing more heterozygous extrapair chicks. Our results suggest that mating patterns may be condition-dependent.     

The effect of climate change on partial migration – the blue tit paradox

Climate change has proven to affect various aspects of the migration of birds. In response to milder winters making the habitat more profitable and increasing the survival of residents, the migratory fraction of partially migratory populations has been predicted to decline. We studied the blue tit Parus caeruleus , a common partial migrant in southern Sweden. The numbers migrating at Falsterbo, a migratory passage site in SW Sweden, has increased during the last decades, in parallel with increasing winter and annual temperatures. Migration data from Falsterbo were compared with yearly indices of the size of the breeding population as estimated by the Swedish National Bird Monitoring Programme. Over the study period 1975–2004, also the breeding population has increased in size. The proportion of blue tits migrating each year did not change over the study period, or possibly even increased slightly, which is in contrast to how climate change has been predicted to influence populations containing both migratory and resident individuals. The most important factors determining the intensity of blue tit migration in a given year was the size of an important winter food source, the beech mast crop (more migrants at lower crops) and the size of the breeding population (more migrants at higher densities).     

The cost of an immune response: vaccination reduces parental effort

A fundamental assumption of theories of the ecology and evolution of inducible defences is that protective responses to attacks by parasites or predators should not only have benefits, but also costs. The vertebrate immune system is by far the best studied example of an inducible defence, yet little is known about the costs of an immune response, especially in natural populations. To test if an immune response per se is costly, we induced an antibody response in female blue tits, Parus caeruleus , by immunising them with human diphtheria–tetanus vaccine, and compared their nestling-feeding rate with that of saline-injected controls. We found that vaccinated females reduced their nestling feeding rate, thus demonstrating a cost of the immune response in the currency of parental effort.     

The blue tit's song is an inconsistent signal of male condition

Sexually selected traits are often hypothesized to signal malecondition or quality, though empirical evidence is mixed, anda number of alternative models of sexual selection do not requirecondition dependence. We examined the relationship between variousmeasures of condition and dawn songs in male blue tits (Cyanistescaeruleus). We detected 6 largely independent measures of variation(i.e., variables) in these songs. None of these variables wererelated to blue tits' ultraviolet–blue plumage, a demonstratedsexual signal, thus failing to support the redundant signalhypothesis. We found some evidence that the song variables wemeasured signaled male quality. There were correlations betweenbody size and certain song traits, though neither male age normale recapture in the subsequent breeding season (apparent localsurvival) predicted any song variation. We combined our resultswith published effect sizes comparing blue tit song with malequality variables using meta-analysis and found that a few songmeasures are correlates of male quality, though as in our fielddata, neither male age nor survival appeared related to song.Our relatively large sample sizes (>60), combined with ourmeta-analytical integration of 89 effect sizes, make the resultsregarding the signaling value of our measured components ofblue tit song robust. These results demonstrate that 1) onlycertain aspects of signal variation may be condition dependentand 2) even when components of a sexual signal appear correlatedwith condition in some studies, these signal components maybe unrelated or inconsistently related to a variety of conditionindices.