Abstract Advances in spring phenology are among the clearest biological responses to climate warming. There has been much interest in how climate impacts on phenology because the timings of key events have implications for species interactions, nutrient cycling and ecosystem services. To date most work has focused on only one aspect of population phenology, the effects of temperature on the average timing. In comparison, effects of temperature on the abundance of individuals and their seasonal spread are understudied, despite their potential to have profound impacts on species interactions. Here we develop a new method that directly estimates the effect of spring temperatures on the timing, height and width of the phenological distribution and apply it to temperate forest caterpillars, a guild that has been the focus of much research on phenology and trophic mismatch. We find that warmer spring conditions advance the timing of the phenological distribution of abundance by −4.96 days °C −1 and increase its height by 34% °C −1 but have no significant effect on the duration of the distribution. An increase in the maximum density of arboreal caterpillars with rising temperatures has implications for understanding climate impacts on forest food chains, both in terms of herbivory pressure and the resources available to secondary consumers. The new method we have developed allows the thermal sensitivity in the full phenological distribution to be modelled directly from raw data, providing a flexible approach that has broad applicability within global change research. Read the free Plain Language Summary for this article on the Journal blog.
This dataset consists of three files: PF_ChoiceDataM.csv: Text file with choice data of male pied flycatchers Samplonius_etal_Rscript.R: The R script used for statistical analysis of the data and creating the graph used in the paper Samplonius_Data_legend_key.pdf: Metadata explaining the variables in the data file
Climate warming has caused the seasonal timing of many components of ecological food chains to advance (Thackeray et al. 2010, 2016). Differential shifts lead to phenological asynchrony, often referred to as trophic mismatch when it is detrimental for consumers (Cushing 1990). In the context of trophic interactions, it has been suggested that consumers will shift their phenology to adapt to shifts in the availability of their food source (Visser and Both 2005), but they rarely do so in practice (Thackeray et al. 2016; Kharouba et al. 2018). Whether such unequal shifts are detrimental or not is unresolved (Johansson and Jonzén 2012; Reed et al. 2013a; Samplonius et al. 2016; Radchuk et al. 2019; Visser and Gienapp 2019). At present there has been no consistent analysis of the links between temperature change, phenological asynchrony, and individual-to-population level impacts across taxa, trophic levels and biomes at a global scale. Instead, many of our insights into mismatch and its impacts stem from a handful of independent single-system studies, varying greatly in their conceptual basis and methodological approach. Here, we propose five criteria that all need to be met to demonstrate that temperature-mediated trophic mismatch poses a growing risk to consumers. These criteria are: 1) an ephemeral resource contributes a large proportion of the consumer’s diet; 2) asynchrony between phenology of consumer and resource is increasing over time; 3) interannual variation in asynchrony is driven by interannual variation in temperature; 4) asynchrony reduces consumer fitness, 5) mismatch impacts negatively on consumer population size or growth. We conduct a literature review of 109 papers studying 132 taxa, and find that for most taxa only two of the five criteria are met. Moreover, all five criteria are only assessed for two taxa. The most commonly-tested criteria are 1 and 2, and few studies further examined evidence for criteria 4 or 5. Furthermore, effects of mismatch are heavily skewed towards juvenile stages rather than adults. Crucially, nearly every study was conducted in Europe or North America, and most studies were on terrestrial secondary consumers. We thus lack a robust evidence base from which to draw general conclusions about the risk that climate-mediated trophic mismatch may pose to populations worldwide.
Establishing the cues or constraints that influence avian timing of breeding is the key to accurate prediction of future phenology. This study aims to identify the aspects of the environment that predict the timing of two measures of breeding phenology (nest initiation and egg laying date) in an insectivorous woodland passerine, the blue tit ( Cyanistes caeruleus ). We analyse data collected from a 220 km, 40-site transect over 3 years and consider spring temperatures, tree leafing phenology, invertebrate availability and photoperiod as predictors of breeding phenology. We find that mean night-time temperature in early spring is the strongest predictor of both nest initiation and lay date and suggest this finding is most consistent with temperature acting as a constraint on breeding activity. Birch budburst phenology significantly predicts lay date additionally to temperature, either as a direct cue or indirectly via a correlated variable. We use cross-validation to show that our model accurately predicts lay date in two further years and find that similar variables predict lay date well across the UK national nest record scheme. This work refines our understanding of the principal factors influencing the timing of tit reproductive phenology and suggests that temperature may have both a direct and indirect effect.
Phenological shifts are well documented biological responses to warming. While many studies have focused on the mean timing of an event, there is growing appreciation that the height and width of the phenological distribution will also impact on species interactions. A temperate deciduous forest food chain of oak trees – arboreal caterpillars – insectivorous passerines has become paradigmatic in research on phenological mismatch. This focus on oak‐dominated woodlands means that we have limited insight into whether 1) caterpillar phenological distributions vary among tree taxa and habitats and 2) oak is an exceptional host, which has implications for the potential for buffering of interactions on a local and landscape scale. Here, we survey caterpillar abundance and mass throughout spring on 10 tree taxa for 10 years across 44 Scottish woodland sites. We found substantial variation in caterpillar abundance among host taxa, with oak, birch and willow yielding similarly high numbers of caterpillars, and evidence that caterpillar abundance increases with the density of oak foliage within a woodland stand, but not with the density of other taxa. Considering variation in the phenological distribution of caterpillars on different host taxa, we found the main axis of variation to be the maximum abundance/total biomass reached, which was highest on oak. We found significant variation in the mean timing of abundance and duration of abundance and total biomass among hosts, though effect sizes were quite small, and little evidence for among host variation in the phenological distribution of individual caterpillar mass. In woodlands where oak is abundant, our findings are consistent with the presence of other tree taxa providing little local buffering of phenological mismatch. Whereas, in the absence of oak, birch and willow have the potential to support similarly substantial caterpillar abundances. These findings have implications for conservation, resilient forestry planting and management decisions.
Social learning allows animals to eavesdrop on ecologically relevant knowledge of competitors in their environment. This is especially important when selecting a habitat if individuals have relatively little personal information on habitat quality. It is known that birds can use both conspecific and heterospecific information for social learning, but little is known about the relative importance of each information type. If provided with the choice between them, we expected that animals should copy the behaviour of conspecifics, as these confer the best information for that species. We tested this hypothesis in the field for Pied Flycatchers Ficedula hypoleuca arriving at their breeding grounds to select a nest box for breeding. We assigned arbitrary symbols to nest boxes of breeding pied flycatchers (conspecifics) and blue and great tits, Cyanistes caeruleus and Parus major (heterospecifics), in 2014 and 2016 in two areas with different densities of tits and flycatchers. After ca 50% of flycatchers had returned and a flycatcher symbol was assigned to their nest box, we gave the later arriving flycatchers the choice between empty nest boxes with either a conspecific (flycatcher) or a heterospecific (tit) symbol.As expected, Pied Flycatchers copied the perceived nest box choice of conspecifics, but only in areas that were dominated by flycatchers. Against our initial expectation, flycatchers copied the perceived choice of heterospecifics in the area heavily dominated by tits, even though conspecific minority information was present.Our results confirm that the relative density of conspecifics and heterospecifics modulates the propensity to copy or reject novel behavioural traits. By contrasting conspecific and heterospecific ecology in the same study design we were able to draw more general conclusions about the role of fluctuating densities on social information use.
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