Parus Major Research Articles

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.

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.

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.

Anatolia: A Hotspot of Avian Genetic Diversity in the Western Palaearctic

Located at the crossroads of two continents and at the southeastern edge of the Mediterranean Basin, Anatolia was one of the most important Pleistocene glacial refugia in the Western Palaearctic. As part of the Irano-Anatolian, Caucasus and Mediterranean Basin biodiversity hotspots, this region is also home to a rich avian community including nearly 400 breeding species. Nevertheless, research addressing the genetic structure and diversity of local bird populations is limited, and information on glacial refugia in this region is still scant, especially when compared to other large Mediterranean peninsulas, namely the Balkan, Italian and Iberian ones. In this study, we contribute to filling this gap by addressing the biogeographic pattern of four common resident songbirds—the Eurasian blue tit (Cyanistes caeruleus), the great tit (Parus major), the Eurasian chaffinch (Fringilla coelebs) and the Eurasian blackbird (Turdus merula)—and one endemic species—the Krüper’s nuthatch (Sitta krueperi)—by amplifying two mitochondrial DNA genes in individuals from Anatolia (n = 329) and comparing their sequences to those of conspecifics from the rest of their distribution range across the western Palaearctic (n = 357) deposited in public databases. The overall genetic structure of these species is consistent with a scenario of isolation for multiple populations in different refugia across Anatolia and subsequent secondary contact in the wake of ice retreat, which makes this region a hotspot of genetic diversity for both widespread and endemic avian species.

Urbanisation-associated shifts in the avian metabolome within the annual cycle

While organisms have evolved to cope with predictable changes in the environment, the rapid rate of current global change presents numerous novel and unpredictable stressors to which organisms have had less time to adapt. To persist in the urban environment, organisms must modify their physiology, morphology and behaviour accordingly. Metabolomics offers great potential for characterising organismal responses to natural and anthropogenic stressors at the systems level and can be applied to any species, even without genomic knowledge. Using metabolomic profiling of blood, we investigated how two closely related species of passerine bird respond to the urban environment. Great tits Parus major and blue tits Cyanistes caeruleus residing in urban and forest habitats were sampled during the breeding (spring) and non-breeding (winter) seasons across replicated sites in southern Sweden. During breeding, differences in the plasma metabolome between urban and forest birds were characterised by higher levels of amino acids in urban-dwelling tits and higher levels of fatty acyls in forest-dwelling tits. The suggested higher rates of fatty acid oxidation in forest tits could be driven by habitat-associated differences in diet and could explain the higher reproductive investment and success of forest tits. High levels of amino acids in breeding urban tits could reflect the lack of lipid-rich caterpillars in the urban environment and a dietary switch to protein-rich spiders, which could be of benefit for tackling inflammation and oxidative stress associated with pollution. In winter, metabolomic profiles indicated lower overall levels of amino acids and fatty acyls in urban tits, which could reflect relaxed energetic demands in the urban environment. Our metabolomic profiling of two urban-adapted species suggests that their metabolism is modified by urban living, though whether these changes represent adaptative or non-adaptive mechanisms to cope with anthropogenic challenges remains to be determined.

How interacting anthropogenic pressures alter the plasticity of breeding time in two common songbirds.

Phenological adjustment is the first line of adaptive response of vertebrates when seasonality is disrupted by climate change. The prevailing response is to reproduce earlier in warmer springs, but habitat changes, such as forest degradation, are expected to affect phenological plasticity, for example, due to loss of reliability of environmental cues used by organisms to time reproduction. Relying on a two-decade, country-level capture-based monitoring of common songbirds' reproduction, we investigated how habitat anthropization, here characterized by the rural-urban and forest-farmland gradients, affected the average phenology and plasticity to local temperature in two common species, the great tit Parus major and the blue tit Cyanistes caeruleus. We built a hierarchical model that simultaneously estimated fledging phenology and its response to spring temperatures based on the changes in the proportion of juveniles captured over the breeding season. Both species fledge earlier in warmer sites (blue tit: 2.94 days/°C, great tit: 3.83 days/°C), in warmer springs (blue tit: 2.49 days/°C, great tit: 2.75 days/°C) and in most urbanized habitats (4 days for blue tit and 2 days for great tit). The slope of the reaction norm of fledging phenology to spring temperature varied across sites in both species, but this variation was explained by habitat anthropization only in the deciduous forest specialist, the blue tit. In this species, the responses to spring temperature were shallower in agricultural landscapes and slightly steeper in more urban areas. Habitat anthropization did not explain variation in the slope of the reaction norm in the habitat-generalist species (great tit), for which mean fledgling phenology and plasticity were correlated (i.e., steeper response in later sites). The effects of habitat change on phenological reaction norms provide another way through which combined environmental degradations may threaten populations' persistence, to an extent depending on species and on the changes in their prey phenology and abundance.

The great tit HapMap project: A continental-scale analysis of genomic variation in a songbird.

A major aim of evolutionary biology is to understand why patterns of genomic diversity vary within taxa and space. Large-scale genomic studies of widespread species are useful for studying how environment and demography shape patterns of genomic divergence. Here, we describe one of the most geographically comprehensive surveys of genomic variation in a wild vertebrate to date; the great tit (Parus major) HapMap project. We screened ca 500,000 SNP markers across 647 individuals from 29 populations, spanning ~30 degrees of latitude and 40 degrees of longitude - almost the entire geographical range of the European subspecies. Genome-wide variation was consistent with a recent colonisation across Europe from a South-East European refugium, with bottlenecks and reduced genetic diversity in island populations. Differentiation across the genome was highly heterogeneous, with clear 'islands of differentiation', even among populations with very low levels of genome-wide differentiation. Low local recombination rates were a strong predictor of high local genomic differentiation (FST), especially in island and peripheral mainland populations, suggesting that the interplay between genetic drift and recombination causes highly heterogeneous differentiation landscapes. We also detected genomic outlier regions that were confined to one or more peripheral great tit populations, probably as a result of recent directional selection at the species' range edges. Haplotype-based measures of selection were related to recombination rate, albeit less strongly, and highlighted population-specific sweeps that likely resulted from positive selection. Our study highlights how comprehensive screens of genomic variation in wild organisms can provide unique insights into spatio-temporal evolutionary dynamics.

Effects of an extreme weather event over reproduction and survival of Great Tits (Parus major) in eastern Spain

AbstractThe frequency of extreme climatic and weather events has increased since 1950 due to global changes induced by human influence. These events can have significant impacts at the individual, population, and community levels across various taxonomic groups. They can be particularly detrimental to bird populations during their breeding season, affecting specific breeding parameters. This study originated from an exceptionally rare breeding season of a resident Great Tit population recorded in spring 2002 when an unusual mortality of nestlings was observed. We quantified weather conditions (temperature, rainfall) from the end of April, a few days before we started detecting failed nests, and compared them with previous and subsequent years. In early May, when many pairs were incubating or caring for newly hatched chicks, we detected unusually low ambient temperatures and unusually high rainfall. This event likely caused that many first clutches failed completely, and that, compared with previous and subsequent years, fledging and breeding success was relatively low in those which were successful. There was also an increased proportion of replacement clutches that year. Anyway, the overall production of fledglings per breeding pair over the breeding season was 2.39, lower than other years. Although recruitment rate in 2003 was similar to other years, the lower production of fledglings in 2002 probably resulted in a decrease in the number of breeding pairs in the following years.

The importance of tree species identity and trait-based winter foraging ecology of bark-foraging bird species in a large Central European floodplain forest

Beyond preferences for particular species of tree, bark-foraging birds are associated with various tree characteristics such as decay stage, trunk diameter, or bark roughness. Our objectives were to study the winter foraging ecology of different bark-foraging bird species in the highly diverse floodplain forests of Donau-Auen National Park (Austria) by examining the importance of tree species and characteristics. We used 'first-foraging' observations on the great spotted woodpecker (Dendrocopos major), middle spotted woodpecker (Leiopicus medius), Eurasian nuthatch (Sitta europaea), treecreepers (Certhia spp.), great tit (Parus major), Eurasian blue tit (Cyanistes caeruleus), and marsh tit (Poecile palustris). We examined bird-tree relationships with a bird-plant network approach, where we compared traits of trees and their preferences among avian species. The five most important tree species relative to distance-weighted fragmentation were European white elm (Ulmus laevis), pedunculate oak (Quercus robur), common ash (Fraxinus excelsior), and white and black poplar (Populus alba, P. nigra). Avian taxa differed only in the use of tree condition, where woodpeckers used decayed and dead trees more than tits. Most species preferred trees of larger trunk diameter with rougher bark. We suspect that changes in these highly diverse floodplain forest stands will eventually lead to changes in bark-foraging bird assemblages. For the protection of such highly diverse floodplain forests, conservation-based water management practices will be crucial to maintaining a sufficient groundwater table. Our findings also suggest that forest management practices should focus on more diverse commercial forest stands with a critical amount of secondary tree species, a variety of size classes, varying tree conditions, and species with different bark roughness classes.

How to solve novel problems: the role of associative learning in problem-solving performance in wild great tits Parus major

Although problem-solving tasks are frequently used to assess innovative ability, the extent to which problem-solving performance reflects variation in cognitive skills has been rarely formally investigated. Using wild breeding great tits facing a new non-food motivated problem-solving task, we investigated the role of associative learning in finding the solution, compared to multiple other non-cognitive factors. We first examined the role of accuracy (the proportion of contacts made with the opening part of a string-pulling task), neophobia, exploration, activity, age, sex, body condition and participation time on the ability to solve the task. To highlight the effect of associative learning, we then compared accuracy between solvers and non-solvers, before and after the first cue to the solution (i.e., the first time they pulled the string opening the door). We finally compared accuracy over consecutive entrances for solvers. Using 884 observations from 788 great tits tested from 2010 to 2015, we showed that, prior to initial successful entrance, solvers were more accurate and more explorative than non-solvers, and that females were more likely to solve the task than males. The accuracy of solvers, but not of non-solvers, increased significantly after they had the opportunity to associate string pulling with the movement of the door, giving them a first cue to the task solution. The accuracy of solvers also increased over successive entrances. Our results demonstrate that variations in problem-solving performance primarily reflect inherent individual differences in associative learning, and are also to a lesser extent shaped by sex and exploratory behaviour.

Breeding parameters of a Great Tit (Parus major) population on the island of Cyprus compared to other Mediterranean populations

Many studies on the Great Tit, Parus major, have been conducted within the Mediterranean Basin, especially on its reproductive biology, forest habitat interactions, and nutritional resources. However, to date no detailed scientific research on these issues has been conducted on the island of Cyprus with a general paucity in research on this topic from the Eastern Mediterranean. Island species, through reduced gene flow and general isolation often evolve reproductive differences from their mainland relatives. As Cyprus is the third largest island in the Mediterranean and the most easterly positioned it provides an ideal opportunity compare the breeding biology of this island population with those from the wider Mediterranean region. This study aimed to gather some baseline reproductive data for Great Tits breeding in Cyprus. This data was then used to compare the reproductive outputs of Cypriot Great Tits from the sub species Parus major aphrodite with other Mediterranean island populations. This study was performed over a 3-year period during the breeding seasons of 2016-2018 in four evergreen forest areas. Mean clutch size was 7.7 eggs and hatching success 76.0%. The mean weight of the young was 16.3 g and mean tarsus length 18.7 mm. Significant differences were found between the years of the study, both in mean clutch size (p<0.0001) and the day of the first egg (p<0.0001), with 2016 producing the largest clutches and clutches being laid earlier than the subsequent two years. The start of the breeding season of the Great Tit was considerably earlier in Cyprus compared to other Mediterranean regions.

Baseline glucocorticoids alone do not predict reproductive success across years, but in interaction with enzymatic antioxidants

AbstractGlucocorticoids are known to adjust organismal functions, such as metabolism, in response to environmental conditions. Therefore, these hormones are thought to play a key role in regulating the metabolically demanding aspects of reproduction, especially in variable environments. However, support for the hypothesis that variation in glucocorticoid concentrations predicts reproductive success is decidedly mixed. Two explanations may account for this discrepancy: (i) Glucocorticoids might not act independently but could interact with other physiological traits, jointly influencing reproduction, and (ii) such an association could become apparent primarily in challenging environments when glucocorticoid concentrations increase. To address these two possibilities, we determined natural variation in circulating baseline glucocorticoid concentrations in parental great tits (Parus major) alongside two physiological systems known to be related with an individual's metabolism: oxidative status parameters (i.e., concentrations of pro‐oxidants, dietary, and enzymatic antioxidants) and body condition. These systems interact with glucocorticoids and can also influence reproductive success. We measured these variables in two breeding seasons that differed in environmental conditions. When accounting for the interaction of baseline glucocorticoids with other physiological traits, we found a positive relationship between baseline glucocorticoids and the number of fledglings in adult great tits. The strength of this relationship was more pronounced for those individuals who also had high concentrations of the enzymatic antioxidant glutathione peroxidase. When studied independently, glucocorticoids were not related to fitness proxies, even in the year with more challenging environmental conditions. Together, our study lend to support the hypothesis that glucocorticoids do not influence fitness alone, but in association with other physiological systems.

Recognizing interspecific dominance signals? Blue tits adjust nest defence based on great tit's black bib size

AbstractAnimals use colours, morphological structures and behaviour to advertise their dominance status and ability to obtain resources (Resource Holding Potential, RHP) in agonistic contexts with conspecifics. Dominance relationships are also known between species, although the interactions and the information used to assess the other species' RHP remain obscure and empirical evidence of interspecific recognition of status is hard to obtain. Using behavioural inference is particularly important when a species needs to assess the potential loss of fitness in terms of reproduction or survival (e.g., risk of damage or predation) that could be inflicted by another species acting as a predator, parasite or competitor. Our study shows for the first time the existence of interspecific recognition of status signals: Blue tits Cyanistes caeruleus (subordinate species) perceive Great tits Parus major (dominant species) as threats as hole‐nesting competitors, and respond differently based on the size of the great tit's black tie stripe. Blue tits seemed to recognize the meaning of great tits' black ties because they were bolder when defending their nests against small‐tie (less dominant) great tits than when repelling attacks by large‐tie (more dominant) great tit males. Our results stress that behavioural inference can potentially be used to assess the meaning of status signals that presumably evolved in an intraspecific signalling context.

Cities as parasitic amplifiers? Malaria prevalence and diversity in great tits along an urbanization gradient

Cities as parasitic amplifiers? Malaria prevalence and diversity in great tits along an urbanization gradient

Environmental harshness does not affect the propensity for social learning in great tits, Parus major

According to the harsh environment hypothesis, natural selection should favour cognitive mechanisms to overcome environmental challenges. Tests of this hypothesis to date have largely focused on asocial learning and memory, thus failing to account for the spread of information via social means. Tests in specialized food-hoarding birds have shown strong support for the effects of environmental harshness on both asocial and social learning. Whether the hypothesis applies to non-specialist foraging species remains largely unexplored. We evaluated the relative importance of social learning across a known harshness gradient by testing generalist great tits, Parus major, from high (harsh)- and low (mild)-elevation populations in two social learning tasks. We showed that individuals use social learning to find food in both colour-associative and spatial foraging tasks and that individuals differed consistently in their use of social learning. However, we did not detect a difference in the use or speed of implementing socially observed information across the elevational gradient. Our results do not support predictions of the harsh environment hypothesis suggesting that context-dependent costs and benefits as well as plasticity in the use of social information may play an important role in the use of social learning across environments. Finally, this study adds to the accumulating evidence that the harsh environment hypothesis appears to have more pronounced effects on specialists compared to generalist species.

Rewriting The Ugly Duckling tale: a Eurasian tree sparrow reared among great tits

Rewriting The Ugly Duckling Tale: a Eurasian tree sparrow reared among great tits. Competitive relationships between hole-nesting passerine bird species can lead to mixed broods when two or more species lay their eggs in the same nest. On 5 May 2023, during a routine inspection of nest boxes in orange plantations in Sagunto, Eastern Spain, we found a Eurasian tree sparrow (Passer montanus) egg dumped among nine great tit (Parus major) eggs. From this clutch, six great tits and the Eurasian tree sparrow hatched, and four great tits and the sparrow fledged. Using a video camera inside the nest box, we observed that the nestlings, including the sparrow, were fed only by great tit adults. The adults brought caterpillars, moths and spiders, a typical great tit nestling diet in this habitat. To date, great tit eggs have been found in Eurasian tree sparrow nests, but to our knowledge this is the first report of a Eurasian tree sparrow chick successfully raised by great tits.

First person – Elisa Thoral

ABSTRACT First Person is a series of interviews with the first authors of a selection of papers published in Biology Open, helping researchers promote themselves alongside their papers. Elisa Thoral is first author on ‘ The relationship between mitochondrial respiration, resting metabolic rate and blood cell count in great tits’, published in BiO. Elisa is a postdoctoral researcher in the lab of Dr Andreas Nord at Lund University, Lund, Sweden, investigating I am interested in the effects of environmental parameters, such as temperature and diet, on animals’ performance at both the organismal and cellular level.

Early developmental carry-over effects on exploratory behaviour and DNA methylation in wild great tits (Parus major).

Adverse, postnatal conditions experienced during development are known to induce lingering effects on morphology, behaviour, reproduction and survival. Despite the importance of early developmental stress for shaping the adult phenotype, it is largely unknown which molecular mechanisms allow for the induction and maintenance of such phenotypic effects once the early environmental conditions are released. Here we aimed to investigate whether lasting early developmental phenotypic changes are associated with post-developmental DNA methylation changes. We used a cross-foster and brood size experiment in great tit (Parus major) nestlings, which induced post-fledging effects on biometric measures and exploratory behaviour, a validated personality trait. We investigated whether these post-fledging effects are associated with DNA methylation levels of CpG sites in erythrocyte DNA. Individuals raised in enlarged broods caught up on their developmental delay after reaching independence and became more explorative as days since fledging passed, while the exploratory scores of individuals that were raised in reduced broods remained stable. Although we previously found that brood enlargement hardly affected the pre-fledging methylation levels, we found 420 CpG sites that were differentially methylated between fledged individuals that were raised in small versus large sized broods. A considerable number of the affected CpG sites were located in or near genes involved in metabolism, growth, behaviour and cognition. Since the biological functions of these genes line up with the observed post-fledging phenotypic effects of brood size, our results suggest that DNA methylation provides organisms the opportunity to modulate their condition once the environmental conditions allow it. In conclusion, this study shows that nutritional stress imposed by enlarged brood size during early development associates with variation in DNA methylation later in life. We propose that treatment-associated DNA methylation differences may arise in relation to pre- or post-fledging phenotypic changes, rather than that they are directly induced by the environment during early development.

Exploring the Impact of Urbanization on Avian Malaria Dynamics in Great Tits: Insights from a Study Across Urban and Non-Urban Environments

Exploring the Impact of Urbanization on Avian Malaria Dynamics in Great Tits: Insights from a Study Across Urban and Non-Urban Environments

The relationship between mitochondrial respiration, resting metabolic rate and blood cell count in great tits.

Although mitochondrial respiration is believed to explain a substantial part of the variation in resting metabolic rate (RMR), few studies have empirically studied the relationship between organismal and cellular metabolism. We therefore investigated the relationship between RMR and mitochondrial respiration of permeabilized blood cells in wild great tits (Parus major L.). We also studied the correlation between mitochondrial respiration traits and blood cell count, as normalizing mitochondrial respiration by the cell count is a method commonly used to study blood metabolism. In contrast to previous studies, our results show that there was no relationship between RMR and mitochondrial respiration in intact blood cells (i.e. with the ROUTINE respiration). However, when cells were permeabilized and interrelation re-assessed under saturating substrate availability, we found that RMR was positively related to phosphorylating respiration rates through complexes I and II (i.e. OXPHOS respiration) and to the mitochondrial efficiency to produce energy (i.e. net phosphorylation efficiency), though variation explained by the models was low (i.e. linear model: R2=0.14 to 0.21). However, unlike studies in mammals, LEAK respiration without [i.e. L(n)] and with [i.e. L(Omy)] adenylates was not significantly related to RMR. These results suggest that phosphorylating respiration in blood cells can potentially be used to predict RMR in wild birds, but that this relationship may have to be addressed in standardized conditions (permeabilized cells) and that the prediction risks being imprecise. We also showed that, in our conditions, there was no relationship between any mitochondrial respiration trait and blood cell count. Hence, we caution against normalising respiration rates using this parameter as is sometimes done. Future work should address the functional explanations for the observed relationships, and determine why these appear labile across space, time, taxon, and physiological state.