Parus Major Research Articles

Social learning is triggered by environmental cues in immigrant birds.

After dispersal, what cues trigger social learning in immigrants? A new study in wild-caught great tits in PLOS Biology suggests that changes in the physical environment, rather than the social environment, are key in prompting social learning by immigrants.

Artificial Light at Night Advances the Onset of Vocal Activity in Both Male and Female Great Tits During the Breeding Season, While Noise Pollution Has Less Impact and Only in Females

Artificial light at night (ALAN) and noise pollution are two important stressors associated with urbanisation that can have a profound impact on animal behaviour and physiology, potentially disrupting biological rhythms. Although the influence of ALAN and noise pollution on daily activity patterns of songbirds has been clearly demonstrated, studies often focus on males, and the few that examined females have not included the potential influence of males on female activity patterns. Using free-living pairs of great tits (Parus major) as a model, we examined for the first time the effects of ALAN and noise pollution and their interaction on the onset of (vocal) activity in both members of a pair. We focused on the egg-laying phase, when both sexes are most vocally active. The onset of male dawn song, female emergence time from the nest box and the onset of female calling in the nest box were measured and used as a proxy for the chronotype. The repeatabilities for all chronotype proxies were high, with higher repeatabilities for males. Consistent with previous studies, ALAN advanced the onset of male dawn song, while it did not elicit a strong response in female emergence time. Additionally, our results suggest an indirect effect of ALAN on the onset of female vocal activity via acoustic interaction with the male. Noise pollution advanced the emergence time in females, while an interaction between ALAN and noise pollution was found for the onset of female calling. In agreement with previous studies, several covariables were shown to have an influence on the activity onset. Taking several proxies for chronotype into account, this study has provided robust evidence of effects of ALAN on male and female cavity-nesting songbirds during the egg-laying period.

Shared environmental similarity between relatives influences heritability of reproductive timing in wild great tits.

Intraspecific variation is necessary for evolutionary change and population resilience, but the extent to which it contributes to either depends on the causes of this variation. Understanding the causes of individual variation in traits involved with reproductive timing is important in the face of environmental change, especially in systems where reproduction must coincide with seasonal resource availability. However, separating the genetic and environmental causes of variation is not straightforward, and there has been limited consideration of how small-scale environmental effects might lead to similarity between individuals that occupy similar environments, potentially biasing estimates of genetic heritability. In ecological systems, environments are often complex in spatial structure, and it may therefore be important to account for similarities in the environments experienced by individuals within a population beyond considering spatial distances alone. Here, we construct multi-matrix quantitative genetic animal models using over 11,000 breeding records (spanning 35 generations) of individually-marked great tits (Parus major) and information about breeding proximity and habitat characteristics to quantify the drivers of variability in two key seasonal reproductive timing traits. We show that the environment experienced by related individuals explains around a fifth of the variation seen in reproductive timing, and accounting for this leads to decreased estimates of heritability. Our results thus demonstrate that environmental sharing between relatives can strongly affect estimates of heritability and therefore alter our expectations of the evolutionary response to selection.

Immigrant birds learn from socially observed differences in payoffs when their environment changes.

Longstanding theory predicts that strategic flexibility in when and how to use social information can help individuals make adaptive decisions, especially when environments are temporally or spatially variable. A short-term increase in reliance on social information under these conditions has been experimentally shown in primates, including humans, but whether this occurs in other taxa is unknown. We asked whether migration between spatially variable environments affected social information use with a large-scale cultural diffusion experiment with wild great tits (Parus major) in captivity, a small passerine bird that can socially learn novel behaviors. We simulated an immigration event where knowledgeable birds were exchanged between groups with opposing preferences for a socially learned foraging puzzle, living in similar or different environments. We found evidence that both immigrants and residents were influenced by social information and attended to the rewards that others received. Our analysis supported the use of a payoff-biased social learning by immigrants when both resources and habitat features were spatially variable. In contrast, immigrants relied more-so on individual learning when payoffs or the environment were unchanged. In summary, our results suggest that great tits assess the payoffs others receive and are more influenced by socially observed differences in payoffs when environmental cues differ in their new environment. Our results provide experimental support for the hypothesis that spatial variability is a strong driver for the evolution of social learning strategies.

Changes of nestling ringing dates in nine bird species over seven decades

Climate change co-occurs with an advancement of avian breeding season (indexed as laying dates or fledging dates) in the temperate zone, suggesting a causality between them. Here, we investigate whether the long-term shifts in nestling (chick) ringing dates also mirror this phenomenon. This index is biased by inherent shortcomings, such as the non-independence of dates (in nestmates, colony members), poor accuracy (long period suitable for ringing), and strange shape of distributions. These shortcomings can be reduced by applying the median of annual ringing dates as an index of breeding phenology. The advantage of this index is that data are available for long periods and large sample sizes. By accepting certain compromise between statistical discipline and fieldwork realities, we examined changes in the breeding phenology of 9 bird species from 1951 to 2020 in Hungary. We found that the annual median of ringing dates advanced significantly (by 9–14 days) in the Black-headed Gull, Common Kestrel, Barn Swallow, Great Tit, and Eurasian Blue Tit. Contrarily, no significant (all P > 0.16) changes occurred in the case of the Common Tern, Black-crowned Night-heron, Common Buzzard, and Long-eared Owl. We also found that the proportion of Great Tits’ second brood has been reduced in recent decades.

Manipulating a host-native microbial strain compensates for low microbial diversity by increasing weight gain in a wild bird population

Empirical studies from laboratory systems and humans show that the gut microbiota is linked to host health. Similar evidence for effects on traits linked to fitness in nature is rare, not least because experimentally manipulating the gut microbiota is challenging. We isolated, characterized, and cultured a bacterial strain, Lactobacillus kimchicus APC4233, directly from a wild bird (the great tit Parus major) and provided it as a self-administered dietary supplement. We assessed the impact of the treatment on the host microbiota community, on weight, and tested whether the treatment affected a previous result linking microbiota alpha diversity to weight in nestlings. The treatment dramatically increased L. kimchicus abundance in the gut microbiota and increased alpha diversity. This effect was strongest in the youngest birds, validating earlier findings pointing to a brief developmental window when the gut microbiota are most sensitive. In time-lagged models, nestling weight was higher in the treatment birds suggesting L. kimchicus may have probiotic potential. There was also a positive time-lagged relationship between diversity and weight in control birds but not in the treatment birds, suggesting L. kimchicus helped birds compensate for low alpha diversity. We discuss why ecological context is likely key when predicting impacts of the microbiome. The manipulation of the gut microbiota with a host native strain in this wild population provides direct evidence for the role of the microbiota in the ecology and evolution of natural populations.

Seasonal variation of birds on a feeding site in a suburban area near Oslo, Norway

The birds visiting a feeding site near a villa in a suburban, residential area in Bærum municipality, west of Oslo, were monitored daily during 1997 - 99, and at irregular intervals during 1993 - 96. Sixteen species had a frequency of more than one week during 1997 - 99. The most common species were: Magpie, Great Tit, Blue Tit, Greenfinch, and Tree Sparrow, all of which occurred during most of the year. There was a clear seasonal pattern in the occurrence of most species. Three species, Siskin, Redpoll, and Brambling, were irregular and occasionally present in relatively large numbers. Invasions occurred especially during cold spells. Among migrant birds, the Blackbird was regularly present during winter. The Robin overwintered irregularly, especially in mild winters.

Individual consistency of hissing displays across night and day in a free-living female songbird

Birds have evolved a variety of antipredator strategies, which have been extensively studied during day-time. Yet, how diurnal birds directly respond to nocturnal predation threats remains largely elusive, despite that predation risk can be high during both night- and day-time. One form of antipredator behaviour found in several tit species when confronted with a predator at the nest is the hissing display. As for many forms of antipredator behaviour, studies on hissing displays have so far focussed on the day-time. Here, we exposed cavity-nesting free-living female great tits (Parus major) to simulated predator intrusions inside their nest box during both night- and day-time. We showed that 28 % of females uttered at least one hissing call during night-time, while the occurrence of hissing calls was higher during day-time (84 %). Hissing females at night, compared to non-hissing females, produced more hissing calls during day-time, providing evidence for individual cross-context consistency. Night-time hissing behaviour did not predict lay date, clutch size, breeding or nest success, indicating the absence of consequences in terms of current reproduction. Together, we reveal the hitherto undescribed occurrence of hissing displays at night in a cavity-nesting bird, while simultaneously strengthening the evidence for the existence of hissing behavioural types.

Anthropogenic noise and light pollution decrease the repeatability of activity patterns and dampen expression of chronotypes in a free-living songbird

Anthropogenic environmental change is introducing a suite of novel disturbance factors, which can have wide-ranging effects on mean behavior and behavioral repeatability. For example, exposure to sensory pollutants, such as anthropogenic noise and artificial light at night (ALAN), may affect consistent and repeatable individual-level timing of daily activity, which is referred to as chronotypes. Although chronotypes have been increasingly documented in wild animal populations and may affect fitness, evidence for long-term stability across life-history stages and seasons is notably lacking. Furthermore, how multiple anthropogenic stressors may interact to erode or magnify the expression of chronotypes remains unclear. We tested for existence of chronotypes across life-history stages and seasons in suburban female great tits (Parus major), using emergence time from nest boxes in the morning as a proxy for activity onset. We then examined joint effects of noise pollution and ALAN on expression of chronotypes, and tested for effects of noise, ALAN, and weather conditions on mean emergence time. We found repeatability of daily activity patterns (emergence times) across life-history stages and seasons, providing evidence of chronotypes, as well as interactive effects of anthropogenic disturbance factors and weather conditions on population mean behavior. Furthermore, across-season repeatability of emergence times was approximately double in magnitude in low light and low noise conditions, relative to in conditions with higher light and/or noise pollution. Thus, joint exposure to these sensory pollutants tends to erode expression of chronotypes. This effect was driven by higher among-individual variance in the relatively undisturbed environment and collapse of this variance in the more disturbed environments. Decreased repeatability in environments with high disturbance levels may reduce potential for behavioral traits, such as chronotype, to be the target of selection and limit adaptability.

Seasonal and between-population variation in heat tolerance and cooling efficiency in a Mediterranean songbird

Discrete populations of widely distributed species may inhabit areas with marked differences in climatic conditions across geographic and seasonal scales, which could result in intraspecific variation in thermal physiology reflecting genetic adaptation, phenotypic plasticity, or both. However, few studies have evaluated inter-population variation in physiological responses to heat. We evaluated within- and inter-population seasonal variation in heat tolerance, cooling efficiency and other key thermoregulatory traits in two Mediterranean populations of Great tit Parus major experiencing contrasting thermal environments: a lowland population subject to hotter summers and a higher annual thermal amplitude than a montane population. Specifically, we measured heat tolerance limits (HTL), body temperature, resting metabolic rate, evaporative water loss, and evaporative cooling efficiency (the ratio between evaporative heat loss to metabolic heat production) within and above the thermoneutral zone during winter and summer. Heat tolerance during summer was greater in lowland than in montane birds; indeed, lowland birds seasonally increased this trait to a significant level, while montane ones did to a lesser extent. Besides, lowland birds showed greater evaporative cooling efficiency during summer (possibly due in part to reductions in total endogenous heat load), while surprisingly montane ones showed the opposite trend. Thus, lowland birds displayed greater seasonal flexibility in HTL, body temperature and resting metabolic rate above thermoneutrality, thus giving some support to the climatic variability hypothesis — that flexibility in thermoregulatory traits should increase with climatic variability. Our results partially support the idea that songbirds’ adaptive thermoregulation in the heat is flexible, highlighting the importance of considering intraspecific variation in thermoregulatory traits when modelling the future distribution and persistence of species under different climate change scenarios.

Did you learn what to eat from your parents? A test of the early learning of the foraging niche hypothesis in great tits Parus major

A growing number of studies suggest that individuals can develop long‐term foraging specializations independently of phenotypic or environmental variation, yet little is known about how the foraging niche is acquired. The early learning of the foraging niche hypothesis suggests a key role of vertical cultural transmission in shaping the foraging niche of vertebrates. In birds, direct evidence from natural conditions is limited to a single study that cross‐fostered two related species. To date, no study has tested whether the diet received as an offspring determines the diet delivered as a parent within a single species. We tested the early learning of the foraging niche hypothesis using a Mediterranean population of great tits Parus major, which show great diet variability and moderate consistency in the diet they provide to their offspring across years. To do this, we recorded prey delivered to 9–14 day‐old chicks over twelve years. Then we assessed vertical transmission of dietary specialization using data (percentage of caterpillars, spiders, and other prey types, as well as mean prey size) from individuals recorded as a chick and as an adult. We standardised the data to control for environmental factors and ran a Linear Model for each prey type to measure individuals' consistency within the group (relative consistency), correlating the diet they received as a chick and the one they provided to their own chicks at the adult stage. The correlations between the diet received as a chick and the diet provided as a parent were either not significant or negative. Hence, although individuals showed relatively consistent foraging niches across years regarding their parental provisioning behaviour, these diet preferences were not correlated to the diet they received in the nest. Further research is needed to determine whether the foraging niche is acquired during the post‐fledgling stage.

Circadian clock period length is not consistently linked to chronotype in a wild songbird.

Circadian clock properties vary between individuals and relate to variation in entrained timing in captivity. How this variation translates into behavioural differences in natural settings, however, is poorly understood. Here, we tested in great tits whether variation in the free-running period length (tau) under constant dim light (LL) was linked to the phase angle of the entrained rhythm ("chronotype") in captivity and in the wild, as recently indicated in our study species. We also assessed links between tau and the timing of first activity onset and offset under LL relative to the last experienced light-dark (LD) cycle. We kept 66 great tits, caught in two winters, in LL for 14 days and subsequently released them with a radio transmitter back to the wild, where their activity and body temperature rhythms were tracked for 1 to 22 days. For a subset of birds, chronotype was also recorded in the lab before release. Neither wild nor lab chronotypes were related to tau. We also found no correlation between lab and wild chronotypes. However, the first onset in LL had a positive relationship with tau, but only in males. Our results demonstrate that links between tau and phase of entrainment, postulated on theoretical grounds, may not consistently hold under natural conditions, possibly due to strong masking. This calls for more holistic research on how the many components of the circadian system interact with the environment to shape timing in the wild. Wild birds showed chronotypes in the field that were unlinked to their circadian period length tau measured in captivity. In males only, the first onset of activity after exposure to constant dim light did correlate with tau. Our study emphasises the need to investigate clocks in the real world, including a need to better understand masking.

Research disturbance negatively impacts incubation behaviour of female great tits

Research disturbance negatively impacts incubation behaviour of female great tits

Per- and Polyfluoroalkyl Substances (PFAS) Accumulation, Reproductive Impairment, and Associations with Nestling Body Condition in Great (Parus major)- and Blue Tits (Cyanistes caeruleus) Living near a Hotspot in Belgium.

Due to the limited number of field studies investigating associations between environmentally relevant per- and polyfluoroalkyl substances (PFAS) mixtures and reproductive impairment, there is uncertainty as to whether birds are affected by PFAS pollution, whether species differ in sensitivity to PFAS, and whether the observed reproductive impairment is caused by PFAS or rather due to other potential confounding variables. Therefore, we investigated PFAS concentrations in eggs and blood plasma of great tit (Parus major) and blue tit (Cyanistes caeruleus) nestlings near a PFAS hotspot in Belgium, reproductive impairment, and associations between the accumulated levels and nestling body condition. In total, 29 eggs and 22 blood plasma samples of great tit clutches, and 10 egg and 10 blood plasma samples of blue tit clutches, were collected. Despite more types of PFAS being detected in eggs compared to plasma, only minor differences in profiles were observed between species. On the other hand, tissue-specific differences were more pronounced and likely reflect a combination of maternal transfer and dietary exposure post-hatching. Despite the high concentrations detected in both species, limited reproductive impairment was observed. Our results support previous findings that great tits and blue tits may not be very susceptible to PFAS pollution and provide evidence that other factors, including ecological stoichiometry, may be more important in explaining inter-species variation in PFAS accumulation and reproductive impairment.

Intrusion of birds into nest cavities depends on the presence of feathers in the cavity and not on species of nest owner

AbstractMost animals live and move in a landscape in which the risk of predation varies spatially and temporally, that is, a “landscape of fear” which may strongly affect their ecology and behaviour. Cavity‐nesting birds prospecting for nest sites are often forced to investigate unfamiliar, dark holes that may be dangerous to enter because they may conceal an aggressive nesting bird or a predator. The Fear of Feathers Hypothesis posits that some birds such as blue tits Cyanistes caeruleus, add large, conspicuous feathers on top of their own nest to exploit the fear of potential nest usurpers or brood parasites. Feathers may trigger fear in prospecting birds either because the feathers obstruct the view of the cavity interior, and/or because the feathers may be perceived as recent prey remains and suggest the predator will return. Here I studied the prospecting behaviour of unmated male pied flycatchers Ficedula hypoleuca by letting them choose between a dyad of nest boxes where one contained a nest of a great tit Parus major and one a nest of a blue tit. The objective was to test whether the presence of feathers would have a stronger repelling effect than the species that had built the nest. Great tits are larger than blue tits and may represent a greater threat to intruding flycatchers. However, blue tits but not great tits, often decorate their nest with large, conspicuous feathers. Consistent with the Fear of Feathers Hypothesis, flycatchers hesitated longer to enter blue tit than great tit nests but only if the blue tit nest contained feathers. The study has relevance to many species of birds that decorate their nest with feathers. It shows that a landscape may include aspects of fear that are important to animal behaviour although they may seem subtle and are easily overlooked.

The Genetic Response of Forest Birds to Urbanization: Variability in the Populations of Great and Blue Tits

The Genetic Response of Forest Birds to Urbanization: Variability in the Populations of Great and Blue Tits

Early-life diet composition affects phenotypic variation of correlated animal personality traits.

Behavioural traits are under both genetic and environmental influence during early life stages. Early environmental conditions related to the amount and type of food have been found to alter behaviour in many organisms. However, how early life diet affects the variation in and the correlation between behavioural traits is largely unknown. Using a multivariate approach, we investigated how variation in parental prey selection is related to three repeatable nestling personality traits, and explored the within and between-individual covariation between these behaviours in a wild passerine, the great tit (Parus major). Our results confirm that breath rate, docility and handling aggression (HA) in great tit nestlings are repeatable traits. Contrary to our expectation, the three nestling personality traits did not form a behavioural 'syndrome' on the phenotypic level in the study population, but we found two of three expected phenotypic correlations, mostly at the within-individual level. Moreover, we found that breath rate significantly decreased with a higher number of spiders in the diet, and docility and handling aggression were significantly and inversely related to higher numbers of noctuids and tortricids in the diets of individuals within broods. Thus, our findings suggest that provisioning quantity and quality during the early life, affects variation in behavioural phenotypes, which occurs mainly at the within-individual level.

Comparative cognition: Free-living birds remember things past

New research suggests that free-living blue and great tits remember foraging, including food type, location, and time since eating, even when event details were not known to be relevant for a subsequent assessment of memory, implicating the use of episodic memory in natural behavior.

Extra-pair paternity and sperm length variation in a far northern Great Tit (Parus major) population

Extra-pair paternity and sperm length variation in a far northern Great Tit (Parus major) population

Extra-pair paternity in two passerine birds breeding in a gradient of urbanisation.

Urbanisation has been increasing worldwide in recent decades, driving environmental change and exerting novel selective pressures on wildlife. Phenotypic differences between urban and rural individuals have been widely documented in several taxa. However, the extent to which urbanisation impacts mating strategies is less known. Here, we investigated extra-pair paternity variation in great tits (Parus major) and blue tits (Cyanistes caeruleus) breeding in nestboxes set in a gradient of urbanisation in Warsaw, Poland, over three breeding seasons. Urbanisation was quantified as the amount of light pollution, noise pollution, impervious surface area (ISA) and tree cover within a 100-m radius around each nestbox. We obtained genotypes for 1213 great tits at 7344 SNP markers and for 1299 blue tits at 9366 SNP markers with a genotyping-by-sequencing method, and inferred extra-pair paternity by computing a genomewide relatedness matrix. We report higher extra-pair paternity in blue tits breeding in more urbanised areas, for example, with higher light pollution and ISA, and lower tree cover. However, no such trend was found in great tits. Late-stage survival of individual nestlings in both species was not associated with paternity or urbanisation proxies, thus we were not able to detect fitness benefits or drawbacks of being an extra-pair offspring in relation to urbanisation. Our results contribute to the growing body of knowledge reporting on the effects of urbanisation on avian ecology and behaviour, and confirm species-specific and population-specific patterns of extra-pair paternity variation.