Captive Great Tits Research Articles

Individual response in body mass and basal metabolism to the risks of predation and starvation in passerines.

Wintering energy management in small passerines has focused on the adaptive regulation of the daily acquisition of energy reserves within a starvation-predation trade-off framework. However, the possibility that the energetic cost of living, i.e. basal metabolic rate (BMR), is being modulated as part of the management energy strategy has been largely neglected. Here, we addressed this possibility by experimentally exposing captive great tits (Parus major) during winter to two consecutive treatments of increased starvation and predation risk for each individual bird. Body mass and BMR were measured prior to and after each week-long treatment. We predicted that birds should be lighter but with a higher metabolic capacity (higher BMR) as a response to increased predation risk, and that birds should increase internal reserves while reducing their cost of living (lower BMR) when exposed to increased starvation risk. Wintering great tits kept a constant body mass independently of a week-long predation or starvation treatment. However, great tits reduced the cost of living (lower BMR) when exposed to the starvation treatment, while BMR remained unaffected by the predation treatment. Energy management in wintering small birds partly relies on BMR regulation, which challenges the current theoretical framework based on body mass regulation.

Integrated molecular and behavioural data reveal deep circadian disruption in response to artificial light at night in male Great tits (Parus major)

Globally increasing levels of artificial light at night (ALAN) are associated with shifting rhythms of behaviour in many wild species. However, it is unclear whether changes in behavioural timing are paralleled by consistent shifts in the molecular clock and its associated physiological pathways. Inconsistent shifts between behavioural and molecular rhythms, and between different tissues and physiological systems, disrupt the circadian system, which coordinates all major body functions. We therefore compared behavioural, transcriptional and metabolomic responses of captive great tits (Parus major) to three ALAN intensities or to dark nights, recording activity and sampling brain, liver, spleen and blood at mid-day and midnight. ALAN advanced wake-up time, and this shift was paralleled by advanced expression of the clock gene BMAL1 in all tissues, suggesting close links between behaviour and clock gene expression across tissues. However, further analysis of gene expression and metabolites revealed that clock shifts were inconsistent across physiological systems. Untargeted metabolomic profiling showed that only 9.7% of the 755 analysed metabolites followed the behavioural shift. This high level of desynchronization indicates that ALAN disrupted the circadian system on a deep, easily overlooked level. Thus, circadian disruption could be a key mediator of health impacts of ALAN on wild animals.

Inferring Whole-Organism Metabolic Rate From Red Blood Cells in Birds.

Metabolic rate is a key ecological variable that quantifies the energy expenditure needed to fuel almost all biological processes in an organism. Metabolic rates are typically measured at the whole-organism level (woMR) with protocols that can elicit stress responses due to handling and confinement, potentially biasing resulting data. Improved, non-stressful methodology would be especially valuable for measures of field metabolic rate, which quantifies the energy expenditure of free-living individuals. Recently, techniques to measure cellular metabolic rate (cMR) in mitochondria of blood cells have become available, suggesting that blood-based cMR can be a proxy of organismal aerobic performance. Aerobic metabolism actually takes place in the mitochondria. Quantifying cMR from blood samples offers several advantages such as direct estimates of metabolism and minimized disturbance of individuals. To our knowledge, the hypothesis that blood-based cMR correlates with woMR has not yet been directly tested. We measured cMR in red blood cells of captive great tits (Parus major), first during their morning activity period and second after subjecting them to a 2.5 h day-time respirometry protocol to quantify woMR. We predicted cMR to decrease as individuals transitioned from an active to a resting state. In the two blood samples we also assessed circulating corticosterone concentrations to determine the perceived disturbance of individuals. From respirometry traces we extracted initial and final woMR measures to test for a predicted positive correlation with cMR measures, while accounting for corticosterone concentrations. Indeed, cMR declined from the first to the second measurement. Furthermore, woMR and cMR were positively related in individuals that had relatively low corticosterone concentrations and displayed little locomotor activity throughout respirometry. By contrast, woMR and cMR covaried negatively in birds that increased corticosterone concentrations and activity levels substantially. Our results show that red blood cell cMR represents a proxy for woMR when birds do not display signs of stress, i.e., either before increases in hormonal or behavioral parameters have occurred or after they have abated. This method represents a valuable tool for obtaining metabolic data repeatedly and in free-living individuals. Our findings also highlight the importance of accounting for individual stress responses when measuring metabolic rate at any level.

Body surface temperature responses to food restriction in wild and captive great tits.

During winter at temperate and high latitudes, the low ambient temperatures, limited food supplies and short foraging periods mean small passerines show behavioural, morphological and physiological adaptations to reduce the risk of facing energy shortages. Peripheral tissues vasoconstrict in low ambient temperatures to reduce heat loss and cold injury. Peripheral vasoconstriction has been observed with food restriction in captivity but has yet to be explored in free-ranging animals. We experimentally food restricted both wild and captive great tits (Parus major) during winter months and measured surface temperatures of the bill and eye region using thermal imaging, to investigate whether birds show rapid local heterothermic responses, which may reduce their thermoregulatory costs when facing a perceived imminent food shortage. Our results of a continuously filmed wild population showed that bill temperature was immediately reduced in response to food restriction compared with when food was available ad libitum, an apparent autonomic response. Such immediacy implies a 'pre-emptive' response before the bird experiences any shortfalls in energy reserves. We also demonstrate temporal variation in vasoconstriction of the bill, with bill temperature gradually rising throughout the food restriction after the initial drop. Eye-region temperature in the wild birds remained at similar levels throughout food restriction compared with unrestricted birds, possibly reflecting the need to maintain steady circulation to the central nervous and visual systems. Our findings provide evidence that birds selectively allow the bill to cool when a predictable food supply is suddenly disrupted, probably as a means of minimising depletion of body reserves for a perceived future shortage in energy.

The Genomics of Circadian Timing in a Wild Bird, the Great Tit (Parus major)

Circadian rhythms are ubiquitous among taxa and are essential for coping with recurrent daily events, leading to selection on the properties of the clock underlying these rhythms. To quantify this selection in the wild, we need, however, to phenotype wild individuals, which is difficult using the standard laboratory approach for which individuals need to be kept under constant conditions. To overcome this problem, we explored the possibility to link the variation in a key clock property, circadian period (Tau), to genetic variation. We measured Tau in 152 captive great tits (Parus major). We further linked Tau to two circadian phase markers, the onset of activity in the Light:Dark cycle, and the first onset in constant conditions (Dim:Dim), directly after entrainment. We did a genome-wide association study using a 650k SNP chip, and we linked genetic polymorphisms of a set of twelve candidate genes, to Tau and the two circadian phase markers. In line with earlier studies, Tau was heritable (h2 =0.48 ± 0.22). Despite this genetic variation, we did not find any significant associations at the genome-wide level with the measured traits and only one candidate gene showed association with onset of activity in the Light:Dark cycle. Identifying the genetic base of circadian timing for wild species thus remains challenging. Including alternative molecular methods such as epigenetics or transcriptomics could help to unravel the molecular basis of the biological clock in great tits.

Personality types vary in their personal and social information use

Gathering information about the environment, such as the location and quality of food, is crucial for an animal's survival, particularly in a changing environment. An animal can collect ‘personal information’ by interacting with the environment itself, or it can collect ‘social information’ by observing the behaviour of others. The use of these two types of information varies across different situations and between individuals. Personality is a concept that captures consistent interindividual differences in behaviour and could be one of the factors driving interindividual variation in information use. We tested this by conducting behavioural experiments based on a colour association task in captive great tits, Parus major, originating from lines bidirectionally selected for high and low exploratory behaviour. We quantified personal information use by measuring to what extent a bird relied on previously rewarded options instead of novel options. Social information use was measured by recording how birds chose according to social information provided by video playbacks of a conspecific. Here, we demonstrate that variation in the use of both personal and social information is indeed personality related. In their decision making, slow explorers relied more on prior knowledge, from both personal and social origins, whereas fast explorers tended to ignore the available information and chose more randomly. The differences between the personality types imply different costs or constraints in acquiring and/or applying the two types of information, possibly due to variation in, for example, cognitive styles. In conclusion, we demonstrate that personality types have different strategies to cope with environmental uncertainty.

Dominance rank and boldness predict social attraction in great tits

Social relationships can have important fitness consequences, and how well an individual is socially connected often correlates with other behavioral traits. Whether such correlations are caused by underlying individual differences in social attraction usually remains unclear, because to identify effects of individual traits on social attraction, it is essential to experimentally exclude the influence of the social partner. Using standardized high-definition video playback on captive great tits (Parus major), we effectively demonstrate the influence of individual traits on the motivation to be near a conspecific. We show that social attraction varied contrastingly with boldness and stimulus novelty. Shyer birds tended to show stronger social attraction when they were confronted with the stimulus bird for the first time. Lower ranked birds showed the overall strongest social attraction. This rank effect remained after experimentally changing dominance ranks by altering group compositions. Moreover, preference for social association tended to increase with a decrease in dominance rank, suggesting that birds plastically change their social preference in relation to their within-group dominance status. Our results provide insight into how social relations can form and change, processes that are key for understanding the long-term consequences of the social environment, and the role individuals might play in influencing this environment themselves.

How Much Variation in the Molt Duration of Passerines can be Explained by the Growth Rate of Tail Feathers?

ABSTRACT. In birds, molt duration is an important trait that can affect plumage functionality and, consequently, the fitness of individuals. However, knowledge about the factors that affect variation in molt speed is sparse, mostly because of the methodological difficulties of studying avian molt. We used a ptilochronology-based approach to estimate the rate at which tail feathers were produced during molt to shed light on the relationship between molt duration and feather growth rate. For that purpose, we used three data sets. First, we tested whether the average molt durations of 22 passerine species were correlated with the mean growth rates of their feathers, using both conventional and phylogenetically corrected statistical procedures. Second, we explored this same association among captive Great Tits (Parus major). And third, we took advantage of the biannual complete molt of Willow Warblers (Phylloscopus trochilus) to examine whether the feathers synthesized during their short summer molt grew fast...

Effects of signal features and environmental noise on signal detection in the great tit, Parus major

Environmental noise caused by human activities may hamper acoustic communication in animals. Field studies in urban environments suggest that birds may alter their communicative behaviour in response to noise, but there is little experimental evidence for a detrimental effect of urban noise on perception. We investigated the masking effects of urban noise on signal detection using operant tests with great tits in the laboratory. We compared masking effects induced by urban noise, woodland noise and a typical dawn chorus, including a variety of singing birds. Maskers were presented at their natural sound pressure level and masking conditions were compared to a silent no-masker condition. The signals to be detected were composed of artificial sinusoids and noise bands mimicking signal features of natural great tit song elements. Both masker condition and signal feature significantly affected signal detection in the captive great tits. Deteriorated auditory thresholds in woodland and urban noise required the signal to be on average 12 dB and 18 dB louder than in the no-masker condition, respectively. The dawn chorus masker showed the most dramatic shift in auditory threshold of about 29 dB. Signals with the sound energy concentrated within a narrow frequency range were on average easier to detect than signals spread over a wide frequency range. Our perceptual results provide insight into how birds may counteract negative masking effects by singing song elements with specific features.

Central assumptions of predator–prey models fail in a semi–natural experimental system

The relationship between the encounter rate of predators with prey and the density of this prey is fundamental to models of predator-prey interactions. The relationship determines, among other variables, the rate at which prey patches are depleted, and hence the impact of predator populations on their prey, and the optimal spatial distribution of foraging effort. Two central assumptions that are made in many models are that encounter rate is directly proportional to prey density and that it is independent of the proportion of prey already removed, other than via the decreased density. We show here, using captive great tits searching for winter moth caterpillars in their natural hiding positions, that neither of these assumptions hold. Encounter rate increased less than directly in proportion to prey density, and it depended not only on the current density of prey, but also on the proportion of prey already removed by previous foragers. Both of these effects are likely to have major consequences for the outcome of predator-prey interactions.

Sight of a Predator Can Stimulate a Corticosterone Response in the Great Tit (Parus major)

The corticosterone response to the sight of a natural predator was investigated in free-living and captive great tits (Parus major). Free-living great tits responded to the sight of a stuffed, slowly moving Tengmalm's owl, a major predator of great tits, with warning calls and a change in behaviour around a feeder. Great tits returned to the feeder within a few minutes and began to approach the owl, and there was no increase in plasma corticosterone levels in birds sampled 30–50 min after they first saw the owl. Captive great tits in an aviary were exposed for 30 min to a stuffed Tengmalm's owl, to a stuffed brambling, and to a cardboard box. All three stimulus objects were slowly rotated during the exposure period. Great tits exposed to the owl changed their behaviour immediately, and spent most of the time when the owl was visible flying around the aviary and hanging from the roof, with very few visits to a feeder. Great tits exposed to the brambling and to the moving box also changed their behaviour and made fewer visits to the feeder. The great tits responded to the sight of the owl with a marked increase in plasma corticosterone levels, whereas there was no change in corticosterone levels (mean levels < 11 ng/ml) in birds exposed to the brambling or to the moving box. Mean corticosterone levels were high (37.1 ± 4.9 ng/ml) 0.5 h after exposure to the owl, remained high (38.9 ± 6.0 ng/ml) 1 h after exposure, and had returned to basal (5.3 ± 1.3 ng/ml) 3 h after exposure to the owl. This is the first demonstration for any bird of a complete corticosterone response to a predator. The sight of a predator initiated a corticosterone response in great tits that could not move more than 3 m away, whereas free-living great tits that could choose how far to fly away from the predator either did not initiate a corticosterone response, or had a small corticosterone response in which corticosterone levels were not significantly different from basal 30–50 min later. The results indicate that the initiation of a corticosterone response in birds depends on whether or not a bird perceives that a stimulus is a threat. Furthermore, they illustrate the importance of not making generalised conclusions based on laboratory experiments.

Variation within and between Birds in Corticosterone Responses of Great Tits (Parus major)

The present study investigated inter- and intraindividual variation of the stress response (in terms of plasma levels of corticosterone) to handling in birds. Individual captive great tits (Parus major) were exposed to a standardised capture and handling protocol three times at about 2-week intervals. Mean plasma corticosterone levels were low (<5 ng/ml) when the birds were first sampled and increased in all birds 10 min after handling (mean levels on each sampling occasion 14 to 22 ng/ml). Levels in some birds then continued to increase, whereas in other birds levels remained relatively constant or had declined 30 min after handling began. Corticosterone responses were measured three times in each bird so that variation in plasma corticosterone levels could be defined. The area under the corticosterone response curve was defined as the integrated corticosterone response and was calculated for each response curve. Variation between birds was quantified by comparing mean values of corticosterone levels and integrated corticosterone responses between birds, then calculating a coefficient of variation for the mean of the individual bird means for each corticosterone parameter. Variation within birds was quantified by calculating the mean of the coefficients of variation for each bird for each corticosterone parameter. Variation in corticosterone levels in the first blood samples at 0 min (coefficient of variation (CV) 84.0%) was greater than variation in peak levels at 10 min (CV 35.1%) and in integrated corticosterone responses (CV 31.9%), indicating that corticosterone responses were more consistent between birds than were basal corticosterone levels. This study has demonstrated that corticosterone responses to a stressor tend to be repeatable in individual great tits, and has provided a method for quantifying variation in corticosterone responses for comparison with other birds in the future.

Individual differences in the use of social information in foraging by captive great tits

We investigated individual differences in copying behaviour of captive great tits, Parus major, by analysing their response to a tutor indicating a new feeding site. We used two groups, each of seven male birds, labelled ‘fast’ and ‘slow’ explorers based on previous studies in which consistent individual differences in the speed of exploring were found. The birds were trained to search for food hidden in a number of differently coloured and shaped feeders, and later to search in only one type of feeder. During the tests, food was absent and the birds were observed in two different situations: alone or in the presence of a tutor, a bird that had been trained to feed in a different kind of feeder. When alone, slow birds readily extended their search to other feeders while fast birds did not change their routine of visiting the previously rewarded ones. In the presence of the tutor, the opposite occurred: slow birds did not change their behaviour while fast birds significantly increased their visits to the feeders indicated by the tutor. Fast and slow individuals thus differ in their foraging and copying behaviour, consistent with the producer–scrounger model.

Prey selection and foraging performance of breeding Great Tits Parus major in relation to food availability

We studied the nestling diet and the foraging performance of Great Tits in relation to prey abundance in the field. Numerous experimental studies present data on foraging decisions in captive Great Tits. Little is, however, known about prey selection in the field in relation to the food available and the consequences this has for the food delivery rate to nestlings. Since the foraging performance of the parents is one of the main determinants of fledging weight and juvenile survival, foraging behaviour is an important part of Great Tit reproduction. During the early breeding season up to 75% of the prey biomass delivered to the nestlings were spiders, which is in contrast with other studies. Only when caterpillars reached a size of 10–12 mg (approximately the average size of the spiders caught at that time) did the Great Tits change their preferences and 80–90% of the delivered prey masses were caterpillars, as reported by other authors. This ‘switching’ between prey occurred within a few days. It was not related to the changes in abundance but to size of caterpillars. The rate at which caterpillars were delivered to the nestlings (in mg/nestling/h) was strongly correlated with the caterpillar biomass available (in mg/m of branches) and nestling growth rate was significantly influenced by the mass of available caterpillars. The results provide evidence why perfect timing of breeding is so important for the Great Tit, and contribute to the understanding of the causal link between food supply, growth and breeding success.

Timing of the Calcium Intake and Effect of Calcium Deficiency on Behaviour and Egg Laying in Captive Great Tits, Parus major

The calcium demand of egg-laying birds is much higher than in other vertebrates during reproduction. We showed elsewhere that a low level of calcium availability can greatly affect the eggshell quality and reproduction of free-living passerines. However, there are few data on calcium demand and calcium intake in relation to egg laying and behaviour and egg-laying performance under conditions of calcium shortage in nondomesticated birds. We examined these aspects in an experiment with captive great tits, Parus major, on a diet deficient in calcium, with or without snail shells as an additional calcium source. More than 90% of the calcium intake for egg production took place during the egg-laying period. Females ingested about 1.7 times as much calcium as they deposited in eggshells. Removing the snail shells after the first egg resulted in eggshell defects and interruptions of laying after 1-3 d. Females without snail shells doubled their searching effort and started to burrow in the soil and to eat sand, small stones, and their own eggs. Most calcium was consumed in the evening, probably to supplement the calcium available from the medullary bone with an additional calcium source in the gut during eggshell formation. The results demonstrated that eggshell formation requires accurate timing of the calcium intake and that obtaining sufficient calcium is time-consuming, even in calcium-rich environments. These factors pertaining to calcium intake greatly affect the ability of birds to collect sufficient calcium for eggshell formation in calcium-poor areas.

Behavioural control of daily fattening in great tits (Parus major)

Many species of temperate-zone passerines show a pronounced daily cycle in body mass. Energy reserves are built up during the day and consumed the following night. The size of reserves is often viewed as a compromise between the risk of starvation and the cost of carrying an excessive fat load. This trade-off calls for state-dependent foraging behaviour, where current reserves and time of day are two crucial factors. The foraging strategy of the birds may then be reflected by the pattern of daily mass gain rate. We temporarily increased energy expenditure in captive great tits (Parus major) by experimentally lowering the overnight temperature. The birds' response to the treatment was to rapidly compensate for reduced morning reserves. Such an increased rate of mass gain suggests state-dependent foraging, and that some feeding opportunities are normally rejected. The rate of return to the normal pattern of fat accumulation suggests that in these birds, foraging is not constrained by physiological limitations.

The relationship between daily routines of singing and foraging: an experiment on captive Great Tits Parus major

Unpaired, singing, male Great Tits Parus major kept in aviaries were subjected to two different daily regimes of foraging profitability. Birds learnt to adjust their foraging patterns to avoid feeding at periods of low foraging profitability. Once learnt, this had no effect on their singing regimes, indicating no direct causal link between the organization of daily regimes of singing and foraging. When first faced with low foraging profitability early in the morning, birds reduced morning song levels but these returned to normal, although no higher than normal, as they learnt to anticipate the daily routine. This suggests that unpredictable periods of low foraging profitability cause reduced singing activity but predictable time of day effects do not. Birds did not spend all their non‐foraging time singing and appeared to have ‘free time’.

Can Great Tits (Parus major) Acquire Search Images?

A 'search image' is said to be acquired when there is change in the ability of a pred'ator to detect cryptic familiar Young great tits Parus major were presented with 'cryptic' and 'conspicuous' artificial prey on bark backgrounds. The results showed that eleven captive great tits had more difficulty detecting cryptic prey than conspicuous prey. Detailed analysis of video recordings revealed two types of search behaviour in response to cryptic prey: (1) the birds sighted (and successfully flew in to take) the prey from vantage points 0.5 m and further away, or (2) they alighted on the bark and then searched over the bark surface in detail. Search images seem to have been acquired when behaviour (1) was used but there was little evidence for search images when behaviour (2) was used. There was a striking difference in the ability of each bird to locate cryptic prey at first as measured by unsuccessful search, overlooking prey, background-directed pecks, followed by accidental discovery, and its ability to detect them as efficiently as conspicuous prey towards the end of its test.

Optimal prey choice and discrimination time in the great tit (Parus major L.)

1. We tested the predictions of an optimal diet model which incorporated time taken to discriminate between prey types. Five captive great tits were presented with a choice of two prey types. The prey were large (profitable) and small (unprofitable) pieces of mealworm inside pieces of plastic drinking straw. 2. When the worms were inside clear plastic straws, the birds selected only large worms, as predicted by the optimal diet model. When the straws were opaque, so that the birds had to spend time discriminating between large and small worms, four out of five individuals became, as predicted, unselective. The fifth individual had a short enough discrimination time for selection to be the optimal policy. 3. An attempt to alter the encounter rate with profitable opaque straws so that birds would resort to selective foraging was not successful because discrimination time for most individuals was too long for the model to predict selection.

The foraging efficiency of great tits ( Parus major L.) in relation to light intensity

I report an experiment aimed at testing whether foraging efficiency of great tits is limited by light intensity at the time of the dawn chorus. Captive great tits hunting for prey under different luminance conditions were less successful in finding prey when foraging, hunted for a lower proportion of their time, and handled individual prey items for longer when luminance was under approximately 7 cd/m 2. This luminance is not reached in the field until after the time of the dawn chorus, suggesting that in the early morning foraging is limited by light intensity. I suggest that a satisfactory functional explanation of the dawn chorus must take into account the comparatively low foraging opportunity early in the morning, as well as the factors affecting the opportunity for singing and other territorial activities.