Parus Major Research Articles

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.

Seasonal and environmental factors contribute to the variation in the gut microbiome: A large-scale study of a small bird.

Environmental variation can shape the gut microbiome, but broad/large-scale data on among and within-population heterogeneity in the gut microbiome and the associated environmental factors of wild populations is lacking. Furthermore, previous studies have limited taxonomical coverage, and knowledge about wild avian gut microbiomes is still scarce. We investigated large-scale environmental variation in the gut microbiome of wild adult great tits across the species' European distribution range. We collected fecal samples to represent the gut microbiome and used the 16S rRNA gene sequencing to characterize the bacterial gut microbiome. Our results show that gut microbiome diversity is higher during winter and thatthere are compositional differences between winter and summer gut microbiomes. During winter, individuals inhabiting mixed forest habitat show higher gut microbiome diversity, whereas there was no similar association during summer. Also, temperature was found to be a small contributor to compositional differences in the gut microbiome. We did not find significant differences in the gut microbiome among populations, nor any association between latitude, rainfall and the gut microbiome. The results suggest that there is a seasonal change in wild avian gut microbiomes, but that there are still many unknown factors that shape the gut microbiome of wild bird populations.

Are comparable studies really comparable? Suggestions from a problem-solving experiment on urban and rural great tits

Performance in tests of various cognitive abilities has often been compared, both within and between species. In intraspecific comparisons, habitat effects on cognition has been a popular topic, frequently with an underlying assumption that urban animals should perform better than their rural conspecifics. In this study, we tested problem-solving ability in great tits Parus major, in a string-pulling and a plug-opening test. Our aim was to compare performance between urban and rural great tits, and to compare their performance with previously published problem solving studies. Our great tits perfomed better in string-pulling than their conspecifics in previous studies (solving success: 54%), and better than their close relative, the mountain chickadee Poecile gambeli, in the plug-opening test (solving success: 70%). Solving latency became shorter over four repeated sessions, indicating learning abilities, and showed among-individual correlation between the two tests. However, the solving ability did not differ between habitat types in either test. Somewhat unexpectedly, we found marked differences between study years even though we tried to keep conditions identical. These were probably due to small changes to the experimental protocol between years, for example the unavoidable changes of observers and changes in the size and material of test devices. This has an important implication: if small changes in an otherwise identical set-up can have strong effects, meaningful comparisons of cognitive performance between different labs must be extremely hard. In a wider perspective this highlights the replicability problem often present in animal behaviour studies.

Episodic-like memory in wild free-living blue tits and great tits

Episodic-like memory in non-human animals represents the behavioral characteristics of human episodic memory-the ability to mentally travel backward in time to "re-live" past experiences. A focus on traditional model species of episodic-like memory may overlook taxa possessing this cognitive ability and consequently its evolution across species. Experiments conducted in the wild have the potential to broaden the scope of episodic-like memory research under the natural conditions in which they evolved. We combine two distinct yet complementary episodic-like memory tasks (the what-where-when memory and incidental encoding paradigms), each targeting a different aspect of human episodic memory, namely the content (what-where-when) and process (incidental encoding), to comprehensively test the memory abilities of wild, free-living, non-caching blue tits (Cyanistes caeruleus) and great tits (Parus major). Automated feeders with custom-built programs allowed for experimental manipulation of spatiotemporal experiences on an individual-level basis. In the what-where-when memory experiment, after learning individualized temporal feeder rules, the birds demonstrated their ability to recall the "what" (food type), "where" (feeder location), and "when" (time since their initial visit of the day) of previous foraging experiences. In the incidental encoding experiment, the birds showed that they were able to encode and recall incidental spatial information regarding previous foraging experiences ("where" test), and juveniles, but not adults, were also able to recall incidentally encoded visual information ("which" test). Consequently, this study presents multiple lines of converging evidence for episodic-like memory in a wild population of generalist foragers, suggesting that episodic-like memory may be more taxonomically widespread than previously assumed.

Nest structure and breeding success in two tit species: a long-term study

AbstractOne of the most critical functions of nests in parids is thermal insulation, particularly during egg incubation by females and during the first week of the hatchlings’ life when they are poikilothermic. Several avian studies reported associations between aspects of breeding success and nest parameters. In this study, we present results regarding long-term (eleven breeding seasons) impact of nest parameters on breeding characteristics in Great Tits (Parus major) and Eurasian Blue Tits (Cyanistes caeruleus) in a deciduous forest and an urban parkland study area. Our findings indicate that in Great Tits and Eurasian Blue Tits the number of fledglings (and in Eurasian Blue Tits also clutch size tended to be) was positively associated with lining mass and was influenced by the study area, with higher values observed in the forest. Additionally, there was a relationship between lining mass and higher hatching success in both tit species. We also demonstrated that both clutch size and number of fledglings were higher in Great Tits in the forest and in Eurasian Blue Tits the number of fledglings was higher in the forest. The study site also impacted hatching success, with Great Tits showing higher rates in the forest, and fledging success for Eurasian Blue Tits being higher in the forest. The number of fledglings differed between years in Great Tits and hatching success and fledging success differed between years in both Great and Eurasian Blue Tit species. We conclude that avian nests play an important role during reproduction, and the materials used to construct nests contribute to various functional properties. However, further studies are needed to establish clear relationships between nest parameters and breeding performance.

Genetic and epigenetic differentiation in response to genomic selection for avian lay date.

Anthropogenic climate change has led to globally increasing temperatures at an unprecedented pace and, to persist, wild species have to adapt to their changing world. We, however, often fail to derive reliable predictions of species' adaptive potential. Genomic selection represents a powerful tool to investigate the adaptive potential of a species, but constitutes a 'blind process' with regard to the underlying genomic architecture of the relevant phenotypes. Here, we used great tit (Parus major) females from a genomic selection experiment for avian lay date to zoom into this blind process. We aimed to identify the genetic variants that responded to genomic selection and epigenetic variants that accompanied this response and, this way, might reflect heritable genetic variation at the epigenetic level. We applied whole genome bisulfite sequencing to blood samples of individual great tit females from the third generation of bidirectional genomic selection lines for early and late lay date. Genomic selection resulted in differences at both the genetic and epigenetic level. Genetic variants that showed signatures of selection were located within genes mostly linked to brain development and functioning, including LOC107203824 (SOX3-like). SOX3 is a transcription factor that is required for normal hypothalamo-pituitary axis development and functioning, an essential part of the reproductive axis. As for epigenetic differentiation, the early selection line showed hypomethylation relative to the late selection line. Sites with differential DNA methylation were located in genes important for various biological processes, including gonadal functioning (e.g., MSTN and PIK3CB). Overall, genomic selection for avian lay date provided insights into where within the genome the heritable genetic variation for lay date, on which selection can operate, resides and indicates that some of this variation might be reflected by epigenetic variants.