4. Shutt, J. D., Nicholls, J. A.,Trivedi, U. H., Burgess, M. D., Stone, G. N., Hadfield, J. D. & Phillimore, A. B. (accepted). Gradients in richness and turnover of a forest passerine’s diet prior to breeding: a mixed model approach applied to faecal metabarcoding data. Mol. Ecol.
Little is known about the dietary richness and variation of generalist insectivorous species, including birds, due primarily to difficulties in prey identification. Using faecal metabarcoding we provide the most comprehensive analysis of a passerine’s diet to date, identifying the relative magnitudes of biogeographic, habitat and temporal trends in the richness and turnover in diet of Cyanistes caeruleus (blue tit) along a 39‐site, 2° latitudinal transect in Scotland. Faecal samples were collected in 2014‐15 from adult birds roosting in nestboxes prior to nest building. DNA was extracted from 793 samples and we amplified COI and 16S minibarcodes. We identified 432 molecular operational taxonomic units (MOTUs) that correspond to putative dietary items. Most dietary items were rare, with Lepidoptera being the most abundant and taxon‐rich prey order. We present a statistical approach for estimation of gradients and inter‐sample variation in taxonomic richness and turnover using a generalised linear mixed model. We discuss the merits of this approach over existing tools and present methods for model‐based estimation of repeatability, taxon richness and Jaccard indices. We find that dietary richness increases significantly as spring advances, but changes little with elevation, latitude or local tree composition. In comparison, dietary composition exhibits significant turnover along temporal and spatial gradients and among sites. Our study shows the promise of faecal metabarcoding for inferring the macroecology of food webs, but we also highlight the challenge posed by contamination and make recommendations of laboratory and statistical practices to minimise its impact on inference.
3. Shutt, J. D., Cabello, I. B., Keogan. K., Leech, D. I., Samplonius, J. M., Whittle, L. Burgess, M. D., & Phillimore, A. B. (2019). The environmental predictors of spatiotemporal variation in the breeding phenology of a passerine bird. Proc. Roy. Soc. B.. (Media: BBC, The Times)
Establishing the cues or constraints that influence avian timing of breeding is 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 220km, 40-site transect over three 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.
2. Shutt, J. D., Burgess, M. D., & Phillimore, A. B. (2019). A spatial perspective on the phenological distribution of the spring woodland caterpillar peak. American Naturalist.
A classic system for studying trophic mismatch focuses on the timing of the spring caterpillar peak in relation to the breeding time and productivity of woodland passerine birds. Most work has been conducted in single-site oak woodlands and little is known about how insights generalise to other woodland types or across space. Here we present the results of a three-year study on the species composition and temporal distribution of the spring caterpillar peak on different tree taxa across 40 woodland sites spanning two degrees of latitude in Scotland. We used molecular barcoding to identify 62 caterpillar species, with winter moth (Operophtera brumata) the most abundant, comprising a third of the sample. Oak (Quercus sp.) and willow (Salix sp.) hosted significantly higher caterpillar abundances than other tree taxa, with winter moth exhibiting similar trends and invariantly proportionate across tree taxa. Caterpillar peak phenology was broadly similar between tree taxa. While latitude had little effect, increasing elevation increased the height of the caterpillar peak and retarded timing by 3.7 days/100m. These findings extend our understanding of how mismatch may play out spatially, with caterpillar peak date varying with elevation, and tree taxa varying in the caterpillar resource that they host.
1. Shutt, J. D., Bolton, M., Cabello, I. B., Burgess, M. D., & Phillimore, A. B. (2018). The effects of woodland habitat and biogeography on blue tit (Cyanistes caeruleus) territory occupancy and productivity along a 220km transect. Ecography.
The nesting phenology and productivity of hole‐nesting woodland passerines, such as tit species (Paridae), has been the subject of many studies and played a central role in advancing our understanding of the causes and consequences of trophic mismatch. However, as most studies have been conducted in mature, oak‐rich (Quercus sp.) woodlands, it is unknown whether insights from such studies generalise to other habitats used by woodland generalist species. Here we applied spatial mixed models to data collected over three years (2014–2016) from 238 nestboxes across 40 sites – that vary in woodland habitat and elevation – along a 220 km transect in Scotland. We evaluate the importance of habitat, biogeography and food availability as predictors of mesoscale among‐site variation in blue tit Cyanistes caeruleus nestbox occupancy and two components of productivity (clutch size and fledging success). We found that habitat was not a significant predictor of occupancy or clutch size but that occupancy exhibited pronounced biogeographic trends, declining with increasing latitude and elevation. However, fledging success, defined as the proportion of a clutch that fledged, was positively correlated with site level availability of birch, oak and sycamore, and tree diversity. The lack of correspondence between the effects of habitat on fledging success versus occupancy and clutch size may indicate that blue tits do not accurately predict the future quality of their breeding sites when selecting territories and laying clutches. We found little evidence of spatial autocorrelation in occupancy or clutch size, whereas spatial autocorrelation in fledging success extends over multiple sites, albeit non‐significantly. Taken together, our findings suggest that the relationship between breeding decisions and breeding outcomes varies among habitats, and we urge caution when extrapolating inferences from one habitat to others.
Selected Related Publications From The Phenoweb Team
Burgess, Malcolm D. and Smith, Ken W. and Evans, Karl L. and Leech, Dave and Pearce-Higgins, James W. and Branston, Claire J. and Briggs, Kevin and Clark, John R. and du Feu, Chris R. and Lewthwaite, Kate and Nager, Ruedi G. and Sheldon, Ben C. and Smith, Jeremy A. and Whytock, Robin C. and Willis, Stephen G. and Phillimore, Albert B. (2018) Tritrophic phenological match-mismatch in space and time. Nature Ecology and Evolution
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.
Samplonius, Jelmer M., Lenka Bartošová, Malcolm D. Burgess, Andrey V. Bushuev, Tapio Eeva, Elena V. Ivankina, Anvar B. Kerimov et al. (2018) Phenological sensitivity to climate change is higher in resident than in migrant bird populations among European cavity breeders. Global Change Biology
Many organisms adjust their reproductive phenology in response to climate change, but phenological sensitivity to temperature may vary between species. For example, resident and migratory birds have vastly different annual cycles, which can cause differential temperature sensitivity at the breeding grounds, and may affect competitive dynamics. Currently, however, adjustment to climate change in resident and migratory birds have been studied separately or at relatively small geographical scales with varying time series durations and methodologies. Here, we studied differential effects of temperature on resident and migratory birds using the mean egg laying initiation dates from 10 European nest box schemes between 1991 and 2015 that had data on at least one resident tit species and at least one migratory flycatcher species. We found that both tits and flycatchers advanced laying in response to spring warming, but resident tit populations advanced more strongly in relation to temperature increases than migratory flycatchers. These different temperature responses have already led to a divergence in laying dates between tits and flycatchers of on average 0.94 days per decade over the current study period. Interestingly, this divergence was stronger at lower latitudes where the interval between tit and flycatcher phenology is smaller and winter conditions can be considered more favorable for resident birds. This could indicate that phenological adjustment to climate change by flycatchers is increasingly hampered by competition with resident species. Indeed, we found that tit laying date had an additional effect on flycatcher laying date after controlling for temperature, and this effect was strongest in areas with the shortest interval between both species groups. Combined, our results suggest that the differential effect of climate change on species groups with overlapping breeding ecology affects the phenological interval between them, potentially affecting interspecific interactions.
Keogan K, Daunt F, Wanless S et al. (2018) Global phenological insensitivity to shifting ocean temperatures among seabirds. Nature Climate Change, 8, 313-318.
Reproductive timing in many taxa plays a key role in determining breeding productivity1, and is often sensitive to climatic conditions2. Current climate change may alter the timing of breeding at different rates across trophic levels, potentially resulting in temporal mismatch between the resource requirements of predators and their prey3. This is of particular concern for higher-trophic-level organisms, whose longer generation times confer a lower rate of evolutionary rescue than primary producers or consumers4. However, the disconnection between studies of ecological change in marine systems makes it difficult to detect general changes in the timing of reproduction5. Here, we use a comprehensive meta-analysis of 209 phenological time series from 145 breeding populations to show that, on average, seabird populations worldwide have not adjusted their breeding seasons over time (−0.020 days yr−1) or in response to sea surface temperature (SST) (−0.272 days °C−1) between 1952 and 2015. However, marked between-year variation in timing observed in resident species and some Pelecaniformes and Suliformes (cormorants, gannets and boobies) may imply that timing, in some cases, is affected by unmeasured environmental conditions. This limited temperature-mediated plasticity of reproductive timing in seabirds potentially makes these top predators highly vulnerable to future mismatch with lower-trophic-level resources.
Phillimore, A. B., Leech, D. I., Pearce‐Higgins, J. W., & Hadfield, J. D. (2016). Passerines may be sufficiently plastic to track temperature‐mediated shifts in optimum lay date. Global Change Biology, 22(10), 3259-3272.
Projecting the fates of populations under climate change is one of global change biology’s foremost challenges. Here, we seek to identify the contributions that temperature‐mediated local adaptation and plasticity make to spatial variation in nesting phenology, a phenotypic trait showing strong responses to warming. We apply a mixed modeling framework to a Britain‐wide spatiotemporal dataset comprising >100 000 records of first egg dates from four single‐brooded passerine bird species. The average temperature during a specific time period (sliding window) strongly predicts spatiotemporal variation in lay date. All four species exhibit phenological plasticity, advancing lay date by 2–5 days °C−1. The initiation of this sliding window is delayed further north, which may be a response to a photoperiod threshold. Using clinal trends in phenology and temperature, we are able to estimate the temperature sensitivity of selection on lay date (B), but our estimates are highly sensitive to the temporal position of the sliding window. If the sliding window is of fixed duration with a start date determined by photoperiod, we find B is tracked by phenotypic plasticity. If, instead, we allow the start and duration of the sliding window to change with latitude, we find plasticity does not track B, although in this case, at odds with theoretical expectations, our estimates of B differ across latitude vs. longitude. We argue that a model combining photoperiod and mean temperature is most consistent with current understanding of phenological cues in passerines, the results from which suggest that each species could respond to projected increases in spring temperatures through plasticity alone. However, our estimates of B require further validation.
Hadfield, J. D. (2016). The spatial scale of local adaptation in a stochastic environment. Ecology Letters, 19(7), 780-788.
The distribution of phenotypes in space will be a compromise between adaptive plasticity and local adaptation increasing the fit of phenotypes to local conditions and gene flow reducing that fit. Theoretical models on the evolution of quantitative characters on spatially explicit landscapes have only considered scenarios where optimum trait values change as deterministic functions of space. Here, these models are extended to include stochastic spatially autocorrelated aspects to the environment, and consequently the optimal phenotype. Under these conditions, the regression of phenotype on the environmental variable becomes steeper as the spatial scale on which populations are sampled becomes larger. Under certain deterministic models – such as linear clines – the regression is constant. The way in which the regression changes with spatial scale is informative about the degree of phenotypic plasticity, the relative scale of effective gene flow and the environmental dependency of selection. Connections to temporal models are discussed.