The effects of climate and habitat on breeding blue tits (Cyanistes caeruleus) and their prey

Ephemeral resource and productivity peaks are characteristic of temperate woodland ecosystems. An ecological model system, which both exhibits and exploits these ephemeral peaks, and is the focus of this thesis, is the deciduous tree-herbivorous caterpillar-insectivorous bird food chain. Phenological synchrony within food chains, displaying ephemeral peaks, is crucial to maximise fitness of higher trophic levels. In the well-studied oak-winter moth-insectivore system, the phenology of all levels are highly temperature sensitive, and given atmospheric warming since the mid-20th century has been, and is predicted to continue, occurring at an unprecedented rate, this tri-trophic system is at risk of phenological mismatch. The effects of climate change on this system have been well studied in oak (Quercus spp.) dominated woodlands across Europe, as oak supports a wide variety of invertebrates. However, little is known about the importance of other deciduous tree species, which also support a variety of invertebrate species that are likely to be important to nesting blue tits (Cyanistes caeruleaus). Understanding the predictors of phenology and productivity across multiple trophic levels is required to understand the pressures on this food chain with a changing climate. The overarching aim of this thesis is to explore the effects of both climate and habitat on the phenology and productivity of both blue tit and herbivorous caterpillars. The effect of tree leafing phenology and air temperature on herbivorous caterpillar phenology was investigated at a local scale, across an extensive woodland site in Durham (UK) through collecting fallen frass. Frass fall phenology was not predicted by temperature or tree phenology, and did not differ across four common deciduous tree species. However, frass fall was most abundant under oak trees, corroborating the importance of oak for Lepidoptera. Across the same Durham study site, nestling blue tits faecal sacs were collected, with a view of using next-generation sequencing to elucidate nestling diet and resource usage, to expand the food chain into a more complex food web. Due to difficulties extracting and amplifying DNA from blue tit nestling faecal sacs, sequencing was unable to be undertaken. However, I provide a method for extracting DNA from difficult faecal samples, which are likely inhibitor-rich and contain highly degraded DNA. The effects of climate and habitat on blue tit phenology and productivity were then considered, by combining bird nesting data from 34 sites across the UK with local temperature and habitat variables. Overall, climatic factors were more important predictors of blue tit phenology and productivity than habitat. Decreased clutch size and earlier breeding phenology, but decreased risk of nest failure, is predicted at higher temperatures. These results, combined, depict a mixed picture for how blue tits may fare with changing climate. To further work presented in this thesis, the effects of climate and habitat on recruitment need to be explored to understand the full implications of the results presented here on blue tit population dynamics

The phenology and clutch size of UK Blue Tits does not differ with woodland composition

The deciduous tree-herbivorous caterpillar-insectivorous bird food chain is a well-studied system for investigating the impacts of climate change across trophic levels. To date, across Europe, most attention has focused on the impacts of increasing spring temperature on changes to phenology in Oak-dominated (Quercus spp.) woodlands. Paridae species and Pied Flycatcher Ficedula hypoleuca are the most studied secondary consumers, all of which demonstrate an advancement in reproductive phenology with increases in spring temperature. Shifts in climate and phenology may also impact on reproductive investment in clutch size, and the effects of climate on phenology and clutch size may vary depending on woodland composition. To date, the effects of among-habitat variation in phenology and reproductive investment have received little attention. Insectivorous birds inhabiting woodlands that differ in tree composition may differ in the timing of breeding, due to local tree leafing phenology acting as a cue for egg-laying date and/or clutch size. Moreover, for most insectivorous birds, woodland composition within a territory is likely to be the main determinant of food availability for both adults and chicks. Consequently, if warming springs affect the temporal patterns of food availability differently across different woodland compositions, this may affect the optimal average local phenology for nesting birds. Here, using data from 34 long-term (mean 15 years) nest monitoring sites across the UK, we investigate the effect of woodland tree composition and temperature on Blue Tit Cyanistes caeruleus first egg date (FED) and clutch size. We supplemented the nest monitoring data by quantifying woodland composition, at a site level, through modified point counts. We predict that birds breeding in woodlands with greater proportions of late-leafing species, such as Oak and Ash Fraxinus excelsior, will breed later than those breeding in woodlands with greater proportions of early-leafing species, such as Birch Betula spp. and Beech Fagus sylvatica. We found no evidence for differences in Blue Tit FED or clutch size in relation to the proportion of any of the tree species investigated, after controlling for temperature and latitude (FED: −3.4 and 2.2, clutch size: −0.4 and − 0.2 eggs for one-unit increase in temperature and latitude, respectively). In recent decades and across all sites, clutch size has decreased as spring temperatures have increased, a strategy which could allow birds flexibly to adjust their breeding phenology such that nestling demand coincides with peak food availability. The lack of an effect of woodland composition on Blue Tit phenology suggests Blue Tits do not fine-tune their reproductive phenology to the local tree composition. Whether this lack of evidence for phenological divergence is due to an absence of divergent selection on breeding phenology and clutch size or to gene flow is not clear

Urbanisation weakens selection on the timing of breeding and clutch size in blue tits but not in great tits

Urbanisation is a globally occurring phenomenon and is predicted to continue increasing rapidly. Urban ecosystems present novel environments and challenges which species must acclimate or adapt to. These novel challenges alter existing or create new selection pressures on behaviours which provide an opportunity to investigate eco-evolutionary responses to contemporary environmental change. We used 7 years of breeding data from urban and forest populations of blue and great tits to understand whether selection for timing of breeding or clutch size differed between the two habitats and species. We found that urban great tits laid eggs earlier than their forest counterparts, but there was no evidence of a difference in selection for earlier breeding. Blue tits, however, did not differ in timing of egg laying between the two habitats, but selection for earlier laying was weaker in the urban environment. Both species laid smaller clutches in the urban site and had positive selection for larger clutch sizes which did not differ in strength for the great tits but did for blue tits, with weaker selection in the urban population. Our results suggest that food availability for nestlings may be constraining urban birds, and that the temporal cues females use to time breeding correctly, such as tree budburst and food availability, may be absent or reduced in urban areas due to lower caterpillar availability. These results have implications for our understanding of the adaptation of wild animals to city life

A global meta-analysis reveals higher variation in breeding phenology in urban birds than in their non-urban neighbours

Cities pose a major ecological challenge for wildlife worldwide. Phenotypic variation, which can result from underlying genetic variation or plasticity, is an important metric to understand eco-evolutionary responses to environmental change. Recent work suggests that urban populations might have higher levels of phenotypic variation than non-urban counterparts. This prediction, however, has never been tested across species nor over a broad geographical range. Here, we conducted a meta-analysis of the avian literature to compare urban versus non-urban means and variation in phenology (i.e. lay date) and reproductive effort (i.e. clutch size, number of fledglings). First, we show that urban populations reproduce earlier and have smaller broods than non-urban conspecifics. Second, we show that urban populations have higher phenotypic variation in laying date than non-urban populations. This result arises from differences between populations within breeding seasons, conceivably due to higher landscape heterogeneity in urban habitats. These findings reveal a novel effect of urbanisation on animal life histories with potential implications for species adaptation to urban environments (which will require further investigation). The higher variation in phenology in birds subjected to urban disturbance could result from plastic responses to a heterogeneous environment, or from higher genetic variation in phenology, possibly linked to higher evolutionary potential

Tritophic phenological match-mismatch in space and time

Increasing temperatures associated with climate change may generate phenological mismatches that disrupt previously synchronous trophic interactions. Most work on mismatch has focused on temporal trends, whereas spatial variation in the degree of trophic synchrony has largely been neglected, even though the degree to which mismatch varies in space has implications for meso-scale population dynamics and evolution. Here we quantify latitudinal trends in phenological mismatch, using phenological data on an oak–caterpillar–bird system from across the UK. Increasing latitude delays phenology of all species, but more so for oak, resulting in a shorter interval between leaf emergence and peak caterpillar biomass at northern locations. Asynchrony found between peak caterpillar biomass and peak nestling demand of blue tits, great tits and pied flycatchers increases in earlier (warm) springs. There is no evidence of spatial variation in the timing of peak nestling demand relative to peak caterpillar biomass for any species. Phenological mismatch alone is thus unlikely to explain spatial variation in population trends. Given projections of continued spring warming, we predict that temperate forest birds will become increasingly mismatched with peak caterpillar timing. Latitudinal invariance in the direction of mismatch may act as a double-edged sword that presents no opportunities for spatial buffering from the effects of mismatch on population size, but generates spatially consistent directional selection on timing, which could facilitate rapid evolutionary change

Feather, but not plasma, glucocorticoid response to artificial light at night differs between urban and forest blue tit nestlings

Urbanization drives phenotypic variation in many animal species. This includes behavioral and physiological traits such as activity patterns, aggression, and hormone levels. A current challenge of urban evolutionary ecology is to understand the environmental drivers of phenotypic variation in cities. Moreover, do individuals develop tolerance to urban environmental factors, which underlie adaptative responses and contribute to the evolution of urban populations? Most available evidence comes from correlative studies and rare experiments where a single urban-related environmental factor has been manipulated in the field. Here we present the results of an experiment in which we tested for differences in the glucocorticoid (CORT) response of urban and rural blue tits nestlings (Cyanistes caeruleus) to artificial light at night (ALAN). ALAN has been suggested to alter CORT response in several animal species, but to date no study has investigated whether this effect of ALAN differs between urban and rural populations. Immediately after hatching, urban and forest broods were either exposed to 2 lux of ALAN (using an LED source mounted inside the nestbox) or received no treatment (dark control). The experiment lasted until the chicks fledged. When the chicks were 13 days old plasma samples were collected to measure baseline CORT concentrations, and feather samples to provide an integrative measure of CORT during growth. Forest birds had higher plasma CORT (pCORT) concentrations than their urban counterparts, irrespective of whether they were exposed to ALAN or not. Conversely, we found population-specific responses of feather CORT to ALAN. Specifically, urban birds that received ALAN had increased feather CORT compared with the urban dark controls, while the opposite was true for the forest birds. pCORT concentrations were negatively associated to fledging success, irrespective of population and treatment, while feather CORT was positively associated to fledging success in broods exposed to ALAN, but negatively in the dark control ones. Our results demonstrate that ALAN can play a role in determination of the glucocorticoid phenotype of wild animals, and may thus contribute to phenotypic differences between urban and rural animals

A global meta‐analysis reveals higher variation in breeding phenology in urban birds than in their non‐urban neighbours

Cities pose a major ecological challenge for wildlife worldwide. Phenotypic variation, which can result from underlying genetic variation or plasticity, is an important metric to understand eco‐evolutionary responses to environmental change. Recent work suggests that urban populations might have higher levels of phenotypic variation than non‐urban counterparts. This prediction, however, has never been tested across species nor over a broad geographical range. Here, we conducted a meta‐analysis of the avian literature to compare urban versus non‐urban means and variation in phenology (i.e. lay date) and reproductive effort (i.e. clutch size, number of fledglings). First, we show that urban populations reproduce earlier and have smaller broods than non‐urban conspecifics. Second, we show that urban populations have higher phenotypic variation in laying date than non‐urban populations. This result arises from differences between populations within breeding seasons, conceivably due to higher landscape heterogeneity in urban habitats. These findings reveal a novel effect of urbanisation on animal life histories with potential implications for species adaptation to urban environments (which will require further investigation). The higher variation in phenology in birds subjected to urban disturbance could result from plastic responses to a heterogeneous environment, or from higher genetic variation in phenology, possibly linked to higher evolutionary potential

Spatiotemporal data on pedunculate oak leafing and peak frass dates for the UK

Data to accompany paper on “Tritrophic mismatch in space and time”. Observations are on the phenology of oak first leaf date and the peak caterpillar frass date across the UK for the period 1998 to 2016.Burgess, Malcolm; Smith, Ken; Leech, David; Pearce-Higgins, J; Branston, Claire; Briggs, Kevin; Clark, John; Evans, Karl; du Feu, Chris; Lewthwaite, Kate; Nager, Ruedi; Sheldon, Ben; Smith, Jeremy; Whytock, Robin; Willis, Stephen; Phillimore, Albert. (2017). Spatiotemporal data on pedunculate oak leafing and peak frass dates for the UK, 1998-2016 [dataset]. University of Edinburgh. http://dx.doi.org/10.7488/ds/2215

Tritrophic phenological match-mismatch in space and time

Increasing temperatures associated with climate change may generate phenological mismatches that disrupt previously synchronous trophic interactions. Most work on mismatch has focused on temporal trends, whereas spatial variation in the degree of trophic synchrony has largely been neglected, even though the degree to which mismatch varies in space has implications for meso-scale population dynamics and evolution. Here we quantify latitudinal trends in phenological mismatch, using phenological data on an oak–caterpillar–bird system from across the UK. Increasing latitude delays phenology of all species, but more so for oak, resulting in a shorter interval between leaf emergence and peak caterpillar biomass at northern locations. Asynchrony found between peak caterpillar biomass and peak nestling demand of blue tits, great tits and pied flycatchers increases in earlier (warm) springs. There is no evidence of spatial variation in the timing of peak nestling demand relative to peak caterpillar biomass for any species. Phenological mismatch alone is thus unlikely to explain spatial variation in population trends. Given projections of continued spring warming, we predict that temperate forest birds will become increasingly mismatched with peak caterpillar timing. Latitudinal invariance in the direction of mismatch may act as a double-edged sword that presents no opportunities for spatial buffering from the effects of mismatch on population size, but generates spatially consistent directional selection on timing, which could facilitate rapid evolutionary change