Temperature synchronizes temporal variation in laying dates across European hole-nesting passerines.

Identifying the environmental drivers of variation in fitness-related traits is a central objective in ecology and evolutionary biology. Temporal fluctuations of these environmental drivers are often synchronized at large spatial scales. Yet, whether synchronous environmental conditions can generate spatial synchrony in fitness-related trait values (i.e., correlated temporal trait fluctuations across populations) is poorly understood. Using data from long-term monitored populations of blue tits (Cyanistes caeruleus, n = 31), great tits (Parus major, n = 35), and pied flycatchers (Ficedula hypoleuca, n = 20) across Europe, we assessed the influence of two local climatic variables (mean temperature and mean precipitation in February-May) on spatial synchrony in three fitness-related traits: laying date, clutch size, and fledgling number. We found a high degree of spatial synchrony in laying date but a lower degree in clutch size and fledgling number for each species. Temperature strongly influenced spatial synchrony in laying date for resident blue tits and great tits but not for migratory pied flycatchers. This is a relevant finding in the context of environmental impacts on populations because spatial synchrony in fitness-related trait values among populations may influence fluctuations in vital rates or population abundances. If environmentally induced spatial synchrony in fitness-related traits increases the spatial synchrony in vital rates or population abundances, this will ultimately increase the risk of extinction for populations and species. Assessing how environmental conditions influence spatiotemporal variation in trait values improves our mechanistic understanding of environmental impacts on populations.

Bird populations most exposed to climate change are less sensitive to climatic variation.

The phenology of many species shows strong sensitivity to climate change; however, with few large scale intra-specific studies it is unclear how such sensitivity varies over a species' range. We document large intra-specific variation in phenological sensitivity to temperature using laying date information from 67 populations of two co-familial European songbirds, the great tit (Parus major) and blue tit (Cyanistes caeruleus), covering a large part of their breeding range. Populations inhabiting deciduous habitats showed stronger phenological sensitivity than those in evergreen and mixed habitats. However, populations with higher sensitivity tended to have experienced less rapid change in climate over the past decades, such that populations with high phenological sensitivity will not necessarily exhibit the strongest phenological advancement. Our results show that to effectively assess the impact of climate change on phenology across a species' range it will be necessary to account for intra-specific variation in phenological sensitivity, climate change exposure, and the ecological characteristics of a population.

Prehatching temperatures drive inter-annual cohort differences in great tit metabolism.

Basal metabolic rate (BMR) constitutes the lowest metabolic rate in a resting animal and is, therefore, considered to reflect the energetic cost of maintenance in endotherms. BMR is a reversible plastic trait that changes with environmental and ecological circumstances, albeit being heritable and susceptible to selection. Inter-individual variation within populations of small birds is substantial, and while many of the drivers of such variation have been identified, many remain unexplained. We studied winter BMR variation of juveniles over a 15-year period in a wild population of great tits Parus major at the northern border of their distribution. BMR during winter consistently changed between years, even after controlling for environmental factors, suggestive of a non-reversible developmental plasticity shaping the adult metabolic phenotype. BMR in cohorts of wintering great tits varied among winters as a response to minimum ambient temperatures experienced early in life, during the prehatching period. This developmental plasticity might be adaptive if temperatures experienced by growing embryos would metabolically prime them to an environment that they will likely encounter in future life. However, in line with a more unpredictable future climate, the risk of phenotype-environment mismatch is likely to lead to certain cohorts being poorly adapted to prevailing winter conditions, resulting in wider annual fluctuations in population size.

Effects of ambient temperatures on evolutionary potential of reproductive timing in boreal passerines.

Many populations need to adapt to changing environmental conditions, such as warming climate. Changing conditions generate directional selection for traits critical for fitness. For evolutionary responses to occur, these traits need to be heritable. However, changes in environmental conditions can alter the amount of heritable variation a population expresses, making predictions about expected responses difficult. The aim of this study was to evaluate the effects of ambient temperatures on evolutionary potential and strength of natural selection on the timing of reproduction in two passerine birds breeding in boreal forests. Long-term data on individually marked Willow Tits Poecile montanus (1975-2018) and Great Tits Parus major (1969-2018) were analysed with random regression animal models to assess if spring temperatures affect the expressed amount of additive genetic variation (VA ) and heritability (h2 ) in the timing of breeding. We assessed if ambient temperatures of different seasons influenced the direction and strength of selection on breeding time. We also evaluated if the strength of selection covaried with evolutionary potential. Levels of VA or h2 expressed in laying date were unaffected by spring temperatures in both study species. Selection for earlier breeding was found in the Willow Tit, but not in the Great Tit. In the Willow Tit, selection for earlier breeding was more intense when the temperatures of following autumns and winters were low. Different measures of evolutionary potential did not covary strongly with the strength of selection in either species. We conclude that there is no or little evidence that climate warming would either constrain or promote evolutionary potential in timing of breeding through changes in amount of genetic variance expressed in boreal Willow and Great Tits. However, selection on the timing of breeding, a life-history event taking place in springtime, is regulated by temperatures of autumns and winters. Rapid warming of these periods have thus potential to reduce the rate of expected evolutionary response in reproductive timing.

From feces to data: A metabarcoding method for analyzing consumed and available prey in a bird-insect food web.

Diets play a key role in understanding trophic interactions. Knowing the actual structure of food webs contributes greatly to our understanding of biodiversity and ecosystem functioning. The research of prey preferences of different predators requires knowledge not only of the prey consumed, but also of what is available. In this study, we applied DNA metabarcoding to analyze the diet of 4 bird species (willow tits Poecile montanus, Siberian tits Poecile cinctus, great tits Parus major and blue tits Cyanistes caeruleus) by using the feces of nestlings. The availability of their assumed prey (Lepidoptera) was determined from feces of larvae (frass) collected from the main foraging habitat, birch (Betula spp.) canopy. We identified 53 prey species from the nestling feces, of which 11 (21%) were also detected from the frass samples (eight lepidopterans). Approximately 80% of identified prey species in the nestling feces represented lepidopterans, which is in line with the earlier studies on the parids' diet. A subsequent laboratory experiment showed a threshold for fecal sample size and the barcoding success, suggesting that the smallest frass samples do not contain enough larval DNA to be detected by high-throughput sequencing. To summarize, we apply metabarcoding for the first time in a combined approach to identify available prey (through frass) and consumed prey (via nestling feces), expanding the scope and precision for future dietary studies on insectivorous birds.

Northward expanding resident species benefit from warming winters through increased foraging rates and predator vigilance.

Species distributions shift northwards due to climate change, but the ecological mechanisms allowing range expansions are not fully understood. Most studies have concentrated on breeding seasons, but winter warming may also be important. Wintering distributions are restricted by food availability and temperature, which may also interact. Foraging in cold conditions requires adaptations as individuals have to be efficient in foraging, while staying warm and vigilant for predators. When the ambient temperature declines, foraging rates should be reduced due to increased time spent on warming behaviours. In addition, predator vigilance should decline, because more time has to be invested in foraging. Cold weather should limit northward expanding southern species in particular, while northern species should perform better in cold conditions. We tested this by studying temperature responses (between 0 and - 35 °C) among wintering birds at feeders. We compared foraging behaviours of two northward expanding southern species, the great tit (Parus major) and the blue tit (Cyanistes caeruleus) to a northern species, the willow tit (Poecile montanus). Foraging rate and vigilance decreased, and warming behaviour increased when temperatures declined. Importantly, the performance in these traits was poorer in the southern species compared to the willow tit. Furthermore, the response to decreasing temperatures in foraging rates and warming behaviour was stronger in the great tits than willow tits. As the winters become warmer, these mechanisms should increase wintering success of southern species wintering at high latitudes, and lead to higher survival, increased population growth, and consequent range expansion.

Different Ultimate Factors Define Timing of Breeding in Two Related Species.

Correct reproductive timing is crucial for fitness. Breeding phenology even in similar species can differ due to different selective pressures on the timing of reproduction. These selection pressures define species' responses to warming springs. The temporal match-mismatch hypothesis suggests that timing of breeding in animals is selected to match with food availability (synchrony). Alternatively, time-dependent breeding success (the date hypothesis) can result from other seasonally deteriorating ecological conditions such as intra- or interspecific competition or predation. We studied the effects of two ultimate factors on the timing of breeding, synchrony and other time-dependent factors (time-dependence), in sympatric populations of two related forest-dwelling passerine species, the great tit (Parus major) and the willow tit (Poecile montanus) by modelling recruitment with long-term capture-recapture data. We hypothesized that these two factors have different relevance for fitness in these species. We found that local recruitment in both species showed quadratic relationships with both time-dependence and synchrony. However, the importance of these factors was markedly different between the studied species. Caterpillar food played a predominant role in predicting the timing of breeding of the great tit. In contrast, for the willow tit time-dependence modelled as timing in relation to conspecifics was more important for local recruitment than synchrony. High caterpillar biomass experienced during the pre- and post-fledging periods increased local recruitment of both species. These contrasting results confirm that these species experience different selective pressures upon the timing of breeding, and hence responses to climate change may differ. Detailed information about life-history strategies is required to understand the effects of climate change, even in closely related taxa. The temporal match-mismatch hypothesis should be extended to consider subsequent critical periods when food needs to be abundantly available.

Different Seasonal Patterns in Song System Volume in Willow Tits and Great Tits.

In most species of seasonally breeding songbirds studied to date, the brain areas that control singing (i.e. the song control system, SCS) are larger during the breeding season than at other times of the year. In the family of titmice and chickadees (Paridae), one species, the blue tit (Cyanistes caeruleus), shows the typical pattern of seasonal changes, while another species, the black-capped chickadee (Poecile atricapillus), shows, at best, very reduced seasonal changes in the SCS. To test whether this pattern holds up in the two Parid lineages to which these two species belong, and to rule out that the differences in seasonal patterns observed were due to differences in geography or laboratory, we compared the seasonal patterns in two song system nuclei volumes (HVC and Area X) in willow tits (Poecile montanus), closely related to black-capped chickadees, and in great tits (Parus major), more closely related to blue tits, from the same area around Oulu, Finland. Both species had larger gonads in spring than during the rest of the year. Great tit males had a larger HVC in spring than at other times of the year, but their Area X did not change in size. Willow tits showed no seasonal change in HVC or Area X size, despite having much larger gonads in spring than the great tits. Our findings suggest that the song system of willow tits and their relatives may be involved in learning and producing nonsong social vocalizations. Since these vocalizations are used year-round, there may be a year-round demand on the song system. The great tit and blue tit HVC may change seasonally because the demand is only placed on the song system during the breeding season, since they only produce learned vocalizations during this time. We suggest that changes were not observed in Area X because its main role is in song learning, and there is evidence that great tits do not learn new songs after their first year of life. Further study is required to determine whether our hypothesis about the role of the song system in the learned, nonsong vocalizations of the willow tit and chickadee is correct, and to test our hypothesis about the role of Area X in the great tit song system.

The relevance of food peak architecture in trophic interactions.

Phenological shifts and associated changes in the temporal match between trophic levels have been a major focus of the study of ecological consequences of climate change. Previously, the food peak has been thought to respond as an entity to warming temperatures. However, food peak architecture, that is, timings and abundances of prey species and the level of synchrony between them, determines the timing and shape of the food peak. We demonstrate this with a case example of three passerine prey species and their predator. We explored temporal trends in the timing, height, width, and peakedness of prey availabilities and explained their variation with food peak architecture and ambient temperatures of prebreeding and breeding seasons. We found a temporal match between the predator's breeding schedule and food availability. Temporal trends in the timing of the food peak or in the synchrony between the prey species were not found. However, the food peak has become wider and more peaked over time. With more peaked food availabilities, predator's breeding success will depend more on the temporal match between its breeding schedule and the food peak, ultimately affecting the timing of breeding in the predator population. The height and width of the food peak depended on the abundances and breeding season lengths of individual prey species and their reciprocal synchronies. Peakednesses of separate prey species' availability distributions alone explained the peakedness of the food peak. Timing and quantity of food production were associated with temperatures of various time periods with variable relevance in different prey species. Alternating abundances of early and late breeding prey species caused high annual fluctuation in the timing of the food peak. Interestingly, the food peak may become later even when prey species' schedules are advanced. Climate warming can thus produce unexpected changes in the food availabilities, intervening in trophic interactions.

Diet shift induced rapid evolution of size and function in a predatory bird.

A predator's body size correlates with its prey size. Change in the diet may call for changes in the hunting mode and traits determining hunting success. We explored long-term trends in sternum size and shape in the northern goshawk by applying geometric morphometrics. Tetraonids, the primary prey of the goshawk, have decreased and been replaced by smaller birds in the diet. We expected that the size of the goshawk has decreased accordingly more in males than females based on earlier observations of outer morphology. We also expected changes in sternum shape as a function of changes in hunting mode. Size of both sexes has decreased during the preceding decades (1962-2008), seemingly reflecting a shift in prey size and hunting mode. Female goshawks hunting also mammalian prey tend to have a pronouncedly "Buteo-type" sternum compared to males preying upon birds. Interestingly, the shrinkage of body size resulted in an increasingly "Buteo-type" sternum in both sexes. In addition, the sternum shape in birds that died accidentally (i.e., fit individuals) was more Buteo-type than in starved ones, hinting that selection was towards a Buteo-type sternum shape. We conclude that these observed patterns are likely due to directional selection driven by changes in the diet towards smaller and more agile prey. On the other hand, global warming is predicted to also cause a decrease in size, thus these two scenarios are inseparable. Because of difficulties in studying fitness-related phenotypic changes of large raptors in the field, time series of museum exemplars collected over a wide geographical area may give answers to this conundrum.

Does the temporal mismatch hypothesis match in boreal populations?

The temporal mismatch hypothesis suggests that fitness is related to the degree of temporal synchrony between the energetic needs of the offspring and their food supply. The hypothesis has been a basis in studying the influence of climate warming on nature. This study enhances the knowledge on prevalence of temporal mismatches and their consequences in boreal populations, and questions the role of the temporal mismatch hypothesis as the principal explanation for the evolution of timing of breeding. To test this, we examined if synchrony with caterpillar prey or timing of breeding per se better explains reproductive output in North European parid populations. We compared responses of temperate-origin species, the great tit (Parus major) and the blue tit (Cyanistes caeruleus), and a boreal species, the willow tit (Poecile montanus). We found that phenologies of caterpillars and great tits, but not of blue tits, have advanced during the past decades. Phenologies correlated with spring temperatures that may function as cues about the timing of the food peak for great and blue tits. The breeding of great and blue tits and their caterpillar food remained synchronous. Synchrony explained breeding success better than timing of breeding alone. However, the synchrony effect arose only in certain conditions, such as with high caterpillar abundances or high breeding densities. Breeding before good synchrony seems advantageous at high latitudes, especially in the willow tit. Thus, the temporal mismatch hypothesis appears insufficient in explaining the evolution of timing of breeding.

Correlation between two components of parental investment: nest defence intensity and nestling provisioning effort of willow tits.

Nest defence intensity and nestling provisioning effort of female willow tits (Parus montanus) were significantly correlated at the end of nestling period: well-fed young were defended most intensely. Increased effort was rewarded, since broods with the highest female per-offspring provisioning rates were the most likely to produce local recruits. This suggests that the feeding ability is an important cue for parental investment decisions, at least in a species like the willow tit which has adopted the clutch adjustment strategy. Thus, the most valuable broods would not necessarily be the largest ones, but the ones in which the original number of young could be fed most adequately. However, no associations were found between the level of parental effort and offspring weight, size or condition, nor did the broods producing recruits differ from other broods in timing of breeding or number and size of offspring. The female behaviour may suggest that they invest the most time, energy and risk in the young whose chances of joining the winter flock are the best. The first well-fed young also gain an advantage of prior residency in joining the flock. The first to join normally obtain higher social status, and hence better winter survival, than latecomers. The corresponding patterns in male parental investment behaviour were weak or absent, which suggested that the male effort was affected by the female behaviour. Males seemed to invest in nestling provisioning in such a way as to supplement the female effort. During nest defence action males also seemed to invest in protection of females against predation.

To breed or not to breed: causes and implications of non-breeding habit in the willow tit Parus montanus.

Causes and consequences of non-breeding in willow tits were studied in northern Finland during 1986-1992. The breeding status was sex and age biased; males and yearling birds were in excess among the non-reproducers. Due to sex bias in the population it appeared detrimental for males to lose a mate, especially shortly before breeding. Lack of a mate was a important factor for males not reproducing (37% of non-breeding males) than for females (14%). Most of the non-breeding birds maintained a pair bond which only rarely broke up for the next breeding season (divorce rate 5.5%). This implies that parental incompatibility is not a possible explanation for pairs not reproducing. Males that did not breed tended to survive better than reproducing ones, whereas such a relationship was not found for females. It is possible that this sex-related difference in survival cost is attributable to quality differences among non-breeding individuals. It was especially low-quality yearling females, with low survival prospects, that were responsible for the discrepancy. The proportion of non-breeding females in the population correlated highly with clutch size and subsequent juvenile survival. It is therefore suggested that for most of these females non-breeding is a phenotypic response to low offspring value in the prevailing circumstances (inter-generational tradeoff). However, it is uncertain whether willow tits in a northern population can use breeding density as an indicator of changing survival prospects of their descendants, as suggested by Ekman and Askenmo (1986) for southern Sweden.