The mechanisms of phenology: the patterns and processes of phenological shifts

Species across a wide range of taxa and habitats are shifting phenological events in response to climate change. While advances are common, shifts vary in magnitude and direction within and among species, and the basis for this variation is relatively unknown. We examine previously suggested patterns of variation in phenological shifts in order to understand the cue-response mechanisms that underlie phenological change. Here, we review what is known about the mechanistic basis for nine factors proposed to predict phenological change (latitude, elevation, habitat type, trophic level, migratory strategy, ecological specialization, species\u27 seasonality, thermoregulatory mode, and generation time). We find that many studies either do not identify a specific underlying mechanism or do not evaluate alternative mechanistic hypotheses, limiting the ability of scientists to predict future responses to global change with accuracy. We present a conceptual framework that emphasizes a critical distinction between environmental (cue-driven) and organismal (response-driven) mechanisms causing variation in phenological shifts and discuss how this distinction can reduce confusion in the field and improve predictions of future phenological change

Adaptive responses of animals to climate change are most likely insufficient

Biological responses to climate change have been widely documented across taxa and regions, but it remains unclear whether species are maintaining a good match between phenotype and environment, i.e. whether observed trait changes are adaptive. Here we reviewed 10,090 abstracts and extracted data from 71 studies reported in 58 relevant publications, to assess quantitatively whether phenotypic trait changes associated with climate change are adaptive in animals. A meta-analysis focussing on birds, the taxon best represented in our dataset, suggests that global warming has not systematically affected morphological traits, but has advanced phenological traits. We demonstrate that these advances are adaptive for some species, but imperfect as evidenced by the observed consistent selection for earlier timing. Application of a theoretical model indicates that the evolutionary load imposed by incomplete adaptive responses to ongoing climate change may already be threatening the persistence of species. © 2019, The Author(s)

Adaptive responses of animals to climate change are most likely insufficient

Biological responses to climate change have been widely documented across taxa and regions, but it remains unclear whether species are maintaining a good match between phenotype and environment, i.e. whether observed trait changes are adaptive. Here we reviewed 10,090 abstracts and extracted data from 71 studies reported in 58 relevant publications, to assess quantitatively whether phenotypic trait changes associated with climate change are adaptive in animals. A meta-analysis focussing on birds, the taxon best represented in our dataset, suggests that global warming has not systematically affected morphological traits, but has advanced phenological traits. We demonstrate that these advances are adaptive for some species, but imperfect as evidenced by the observed consistent selection for earlier timing. Application of a theoretical model indicates that the evolutionary load imposed by incomplete adaptive responses to ongoing climate change may already be threatening the persistence of species.Peer reviewe

The influence of spatial and temporal climate variation on species' distributions, phenologies and interactions

With climate change, species are shifting their distributions polewards and upwards, and advancing their phenologies. However, there is substantial interspecific variation in these responses and ecologists are having difficulty explaining why. Understanding this variation is critical as it is likely to lead to widespread consequences for trophic interactions and ecological communities. In this thesis, I test several hypotheses concerning the causes and ecological consequences of interspecific and intertaxonomic variation in climate-distribution and phenology-temperature relationships. First, I tested and found support for the hypothesis that species from different taxonomic groups vary in the strength of climate-distribution relationships, likely because of differences in their life history strategies. However, my results suggest that dispersal ability is unlikely to be the key trait affecting species' geographic distributions at broad scales. Across broad-scales, I found that butterfly and plant phenologies were strongly affected by temperature, suggesting that phenological shifts in response to future climate change are likely to be widespread. Flight season timing of early-season butterfly species and those with lower dispersal ability was more sensitive to temperature than later-season species and those with greater dispersal ability, suggesting that ecological traits can account for some of the interspecific variation in phenological sensitivity to temperature. Differences in phenological sensitivities of butterflies and plants to temperature imply that shifts in phenological synchrony are likely and could be substantial for interacting species, potentially resulting in important fitness consequences. Finally, experimentally warming the egg masses and larvae of the western tent caterpillar (Malacosoma californicum pluviale) placed on the branches of its host plant, red alder (Alnus rubra), in the field led to opposing direct and indirect effects on larval development. Warming significantly advanced larval but not leaf emergence, which initially prolonged larval development. However, once leaves were present, warming accelerated larval development, resulting in no overall effects on larval development. Taken together, this thesis demonstrates that to understand the full implications of climate change for species and communities, accounting for species' life history strategies and interactions will be essential. However, without more quantitative estimates of the fitness consequences of shifts in phenological synchrony, this understanding will be limited.Science, Faculty ofZoology, Department ofGraduat

Phenological sensitivity to temperature at broad scales: opportunities and challenges of natural history collections

The seasonal timing of biological events (i.e. phenology) has been frequently observed to shift in response to recent climate change. While many of these events now occur earlier due to warmer temperatures, there is considerable variation in the direction and magnitude of these shifts across species. This variation could have consequences for species interactions and ecological communities, especially when the relative timing of key life cycle events among species is disrupted. As a first step to better understand the causes and consequences of variation in species’ phenological responses to climate change, we used natural history collections to quantify and compare broad-scale patterns in phenology-temperature relationships for Canadian butterflies and their nectar food plants over the past century. The phenology of both groups advanced in response to warmer temperatures - both across years and sites. Across butterfly-plant associations, flowering time was significantly more sensitive to temperature than the timing of butterfly flight. However, the sensitivities were not correlated across associations. The findings we will present indicate that warming-driven shifts in the timing of species interactions are likely to be prevalent. The opportunities and challenges associated with using natural history collections for detecting and linking phenological responses to climate change will also be discussed

Data from: Flowering time of butterfly nectar food plants is more sensitive to temperature than the timing of butterfly adult flight

1. Variation among species in their phenological responses to temperature change suggests that shifts in the relative timing of key life cycle events between interacting species are likely to occur under climate warming. However, it remains difficult to predict the prevalence and magnitude of these shifts given that there have been few comparisons of phenological sensitivities to temperature across interacting species. 2. Here, we used a broad-scale approach utilizing collection records to compare the temperature sensitivity of the timing of adult flight in butterflies vs. flowering of their potential nectar food plants (days per °C) across space and time in British Columbia, Canada. 3. On average, the phenology of both butterflies and plants advanced in response to warmer temperatures. However, the two taxa were differentially sensitive to temperature across space vs. across time, indicating the additional importance of nontemperature cues and/or local adaptation for many species. 4. Across butterfly–plant associations, flowering time was significantly more sensitive to temperature than the timing of butterfly flight and these sensitivities were not correlated. 4. Our results indicate that warming-driven shifts in the relative timing of life cycle events between butterflies and plants are likely to be prevalent, but that predicting the magnitude and direction of such changes in particular cases is going to require detailed, fine-scale data

Phenological data for select plant species in British Columbia, Canada

This data was compiled from the University of British Columbia Herbarium. Each row represents a specimen that was in flower at the time of collection. 'Accession' is the unique identifier associated with the specimen that is found in the herbarium database. 'Vegetation' is the type of vegetation (tree, shrub, herbaceous). 'Family' is the species' family. 'Day/month/year' is the date associated with the specimen. 'x' is the longitude and 'y' is the latitude associated with the record. These coordinates were either listed directly on the specimen or achieved by georeferencing by the museum or by the authors. Georeferencing was done using locality descriptions on the specimen. 'Uncertainty (in meters)' is the uncertainty associated with the geographic coordinates achieved by georeferencing that was quantified whenever possible

Anthropogenic disturbance promotes the abundance of a newly introduced butterfly in Canada, Polyommatus icarus (Lepidoptera: Lycaenidae)

The frequency of introductions of non-native species is increasing worldwide, but only a few introduced species undergo rapid population growth and range expansion, and even fewer become invasive, leading to negative impacts on native communities. Predicting which non-native species are likely to become widespread and abundant can be difficult when there is a lack of species’ information in the early stages of colonization. Here, we investigate the ecology of a newly introduced butterfly in Canada, the European Common Blue (Polyommatus icarus Rottemberg, 1775), by modelling its local- and landscape-scale habitat suitability in Montral, Canada and the surrounding region, and by assessing its dispersal ability using a mark-release-recapture study. At a local-scale, we found that P. icarus abundance was highest at sites with moderate levels of habitat disturbance (e.g., mowed every 2-3 years), the presence of their preferred larval host plant and low proportional cover of grasses. At a landscape-scale, P. icarus abundance increased with an increasing proportion of urban area and decreasing proportion of forests. We also found that P. icarus is a low to mid-level disperser relative to other butterflies. Our results suggest that P. icarus may become widespread in disturbed and urban areas across Canada, but that further investigation into additional potential range-constraining factors (e.g., microclimate), especially larval preferences, and modelling of the trajectory of P. icarus range expansion is needed.The accepted manuscript in pdf format is listed with the files at the bottom of this page. The presentation of the authors' names and (or) special characters in the title of the manuscript may differ slightly between what is listed on this page and what is listed in the pdf file of the accepted manuscript; that in the pdf file of the accepted manuscript is what was submitted by the author

Disentangling the direct, indirect, and combined effects of experimental warming on a plant–insect herbivore interaction

There is increasing evidence that climate warming will have both direct and indirect effects on species. Whereas the direct effects of climate warming represent the proximate physiological consequences of changing abiotic conditions, the indirect effects of climate change reflect changes mediated by at least one other interacting species. The relative importance of these two kinds of effects has been unclear, limiting our ability to generalize the response of different species to climate change. Here, we used a series of experiments to disentangle some of the key direct and indirect effects of warming on the growth of monarch butterfly caterpillars (Danaus plexippus) and showy milkweed plants (Asclepias speciosa) during a window of rapid growth for both species. The effects of warming differed between direct, indirect, and combined effect experiments. Warming from 26°C to 30°C directly increased the growth of both monarch larvae and milkweeds, with monarch and milkweed growth rates showing similar sensitivity to warming. However, in a subsequent experiment, we did not observe significantly increased growth when comparing caterpillars and plants reared at 27°C and 31°C, suggesting that small differences can change the direct effects of warming. When caterpillars that were maintained at laboratory temperatures were fed leaves from host plants that were exposed to warmer temperatures, warming had a negative indirect effect on larval growth rates likely mediated by decreases in milkweed leaf quality. In experiments combining direct and indirect effects, we observed a net positive effect of warming on larval growth rates. Warming had no combined effects on milkweed growth, potentially due to opposing positive direct and negative indirect effects on growth mediated via increased monarch herbivory. These results show how variability among the direct, indirect, and combined effects of even relatively simple, short-term climatic perturbations can present challenges for predicting the broader effects of climatic warming in multispecies communities