Full phenological distribution and the match/mismatch hypothesis

Shifts in the timing of key life history events are some of the most documented biological responses to climate warming. Synchronous timing between a consumer and ephemeral resource can be important for consumer fitness, with asynchrony between the two parties often having a negative effect, as outlined by the match-mismatch hypothesis (MMH). Differences in the thermal sensitivity of phenology among species occupying different trophic levels leave consumers at risk of asynchrony within time-sensitive trophic interactions under climate warming. There is abundant evidence that secondary consumers shift their phenology by less than their resources, resulting in them lagging behind the resource as temperatures increase. As such, phenology and the MMH have become prominent in research regarding the impacts of climate warming on biological systems. The phenology of individuals within a population is often summarised using the mean. However, interactions are not just sensitive to the mean of each trophic level, but instead the synchrony among individuals. The range of timings among individuals forms the phenological distribution, described by the maximum number of individuals (height), the range of dates over which the event will occur (duration), and the relative shape (width). Differences in the height, duration and width of the phenological distribution of an ephemeral resource are likely to have implications for the MMH, affecting the prevalence of food available to the consumer at any point in time, and also at different levels of asynchrony to the mean timing of the resource. For example, with a wider resource distribution, the difference in food available to synchronous consumers versus asynchronous consumers will be less than when there is a narrower resource distribution. As such, if the fitness of consumers is affected by variation in the phenological distribution of food availability, differences in the distribution of a resource could affect consumer mean population fitness and the strength of selection on timing. Given the possible implications that shifts in these aspects of the full phenological distribution have for trophic interactions, it is surprising that it has been the focus of minimal research to date. In this thesis, I utilise data on the spring peak in arboreal caterpillars within deciduous woodland systems and the breeding phenology and breeding success of blue tits (Cyanistes caeruleus). I explore variations in the phenological distribution of caterpillars and the implications for the phenological fitness function of blue tits, an insectivorous bird that relies on caterpillars to feed young. Data have been collected across 44 sites spanning an elevation range of 10-433m and 2o latitude through Scotland over nine years. The sites vary both in woodland tree composition and in temperature. In Chapter 1, I introduce phenology, the MMH, the full phenological distribution and the deciduous woodland study system. Chapters 2 and 3 then focus on habitat and temperature as drivers of the phenological distribution of caterpillars. In Chapter 4, I examine the consequences of the full phenological distribution of caterpillars for blue tit fitness relative to breeding phenology, and in Chapter 5 I discuss the broader implications of my work, limitations and future directions and opportunities. In Chapter 2 I examine variation in the phenological distribution of caterpillars in relation to woodland tree composition using data on the abundance and mass of caterpillars on ten different tree taxa throughout spring, and information about the local tree taxa composition more specifically. I find that there is substantial variation in the abundance of caterpillars supported by different deciduous tree taxa and that the prevalence of oak trees in the local woodland has an additional effect, increasing the abundance of caterpillars found throughout the site. I also found that there is substantial variation in the height of the caterpillar peak hosted by different tree taxa, and some minimal variation in the timing of the peak and the duration. There was no significant difference in the ultimate mass of caterpillars among taxa meaning that the differences in the peak in biomass among tree taxa largely mirrored patterns seen for the peak in abundance. These results show that woodland tree composition contributes to variation in the phenological distribution of caterpillars between locations, suggesting that studying the MMH in a range of woodland types may be of benefit to accurately predict the consequences of climate warming at the meta-population level. In Chapter 3, I identified the time periods within spring during which average temperature best predicted the timing, height and width of the phenological distribution of caterpillar abundance. I found mean timing to be better predicted by temperatures earlier in spring with height predicted by temperatures that were slightly later, whilst there was substantial uncertainty in the period over which average temperature best predicted width. In this chapter I develop a novel method to phenology research, testing for thermal sensitivity in the mean timing, height and width of the phenological distribution of caterpillars from raw data of abundance over time. I found that the height of the phenological distribution increases substantially with an increase in temperature and that the shape becomes more steeply peaked, falling over a similar duration of time. These results suggest climate warming is having a substantial impact on the phenological distribution of a key resource in temperate woodlands and provides additional insights into the impacts of climate change past shifts in mean timing alone. In Chapter 4 I present an extension to the MMH in which the full phenological distribution of caterpillars affects the full phenological fitness function of blue tits. I achieve this by extending the statistical method from Chapter 3 and use site and year specific estimates of the mean timing, height and width of the caterpillar peak to predict the equivalent metrics in the blue tit fledging success fitness function. This framework has the potential to allow tests of how the timing of the caterpillar peak affects the optimal breeding timing for blue tits, whether the maximum height of the caterpillar peak affects the maximum fitness of blue tits, and whether the width of the caterpillar peak affects the width of the phenological fitness function which may have implications for the strength of selection. However, having identified no optimum hatch date for blue tits within the fledging success data, the data do not conform with the structure of the framework described. As an alternative, I examined the effect of the mean timing, height and width of the caterpillar phenological distribution among site by year combinations on a straight-line fitness function for the birds, allowing the intercept and slope of fledging success over time to vary with each caterpillar parameter. I found no effect of the mean timing, height or width of the caterpillar peak on the blue tit phenological fitness function which shows no evidence of the MMH affecting these populations. Alternatively, I suggest parental quality may have a stronger effect than environmental factors on fledging success. As the effect of the MMH has varied among fitness traits in other passerine species this does not rule out any effect of the phenological distribution extension of the MMH, but presents an opportunity for further work on this topic. Nevertheless, the conceptual framework put forwards holds an interesting progression for how we perceive the dynamics within these ephemeral trophic interactions. In this thesis, I have introduced approaches that allow more nuanced insights into the impacts of climate change on phenology and the consequences of phenology for fitness. The phenological distribution of caterpillars varies with woodland tree composition, contributing to spatial heterogeneity in a key resource and guild of herbivores. The increase in height and narrowing shape of the phenological distribution with an increase in temperature shows that reducing the caterpillar peak to mean timing misses important information about how the resource is responding to a warming climate. By extending the conceptual framework of the MMH we gain insight into how the resource distribution can influence the strength of selection and population persistence, highlighting the value of considering the full phenological distribution in phenology and MMH research. The theory and statistical methods employed in this thesis are transferable to a vast range of species and interactions. To accurately interpret and predict the impacts of climate warming in biomes driven by the strong seasonality of events, it may be essential to move on from focusing on mean timing and begin to incorporate the full phenological distribution.