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

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

Growing degree‐days do not explain moth species' distributions at broad scales

Abstract Growing degree‐days (GDD), an estimate of an organism's growing season length, has been shown to be an important predictor of Lepidopteran species' distributions and could be influencing Lepidopteran range shifts to climate change. Yet, one understudied simplification in this literature is that the same thermal threshold is used in the calculations of GDD for all species instead of a species‐specific threshold. By characterizing the phenological process influenced by climate, a species‐specific estimate of GDD should improve the accuracy of species distribution models (SDMs). To test this hypothesis, we used published, experimentally estimated thermal thresholds and modeled the current geographic distribution of 30 moth species native to North America. We found that the predictive performance of models based on a species‐specific estimate of GDD was indistinguishable from models based on a standard estimate of GDD. This is likely because GDD was not an important predictor of these species' distributions. Our findings suggest that experimentally estimated thermal thresholds may not always scale up to be predictive at broad scales and that more work is needed to leverage the data from lab experiments into SDMs to accurately predict species' range shifts in response to climate change

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

Autumn larval cold tolerance does not predict the northern range limit of a widespread butterfly species

Abstract Climate change is driving range shifts, and a lack of cold tolerance is hypothesized to constrain insect range expansion at poleward latitudes. However, few, if any, studies have tested this hypothesis during autumn when organisms are subjected to sporadic low‐temperature exposure but may not have become cold‐tolerant yet. In this study, we integrated organismal thermal tolerance measures into species distribution models for larvae of the Giant Swallowtail butterfly, Papilio cresphontes (Lepidoptera: Papilionidae), living at the northern edge of its actively expanding range. Cold hardiness of field‐collected larvae was determined using three common metrics of cold‐induced physiological thresholds: the supercooling point, critical thermal minimum, and survival following cold exposure. P. cresphontes larvae were determined to be tolerant of chilling but generally die at temperatures below their SCP, suggesting they are chill‐tolerant or modestly freeze‐avoidant. Using this information, we examined the importance of low temperatures at a broad scale, by comparing species distribution models of P. cresphontes based only on environmental data derived from other sources to models that also included the cold tolerance parameters generated experimentally. Our modeling revealed that growing degree‐days and precipitation best predicted the distribution of P. cresphontes, while the cold tolerance variables did not explain much variation in habitat suitability. As such, the modeling results were consistent with our experimental results: Low temperatures in autumn are unlikely to limit the distribution of P. cresphontes. Understanding the factors that limit species distributions is key to predicting how climate change will drive species range shifts

Low prevalence of the parasite Ophryocystis elektroscirrha at the range edge of the eastern North American monarch (Danaus plexippus) butterfly population

Every year monarch butterflies (Danaus plexippus Linnaeus, 1758) from the eastern North American population migrate from Mexico to Southern Canada in the spring. This northward migration has been shown to reduce monarch infection with the host-specific parasite Ophryocystis elektroscirrha (OE) (McLaughlin and Myers, 1970); yet, the prevalence of OE at their range limits, and the mechanism(s) responsible, is unknown. We assessed OE infection levels of monarchs at the northern edge of the eastern population distribution around Ottawa, Canada, and found extremely low levels of infection (~1% with upper confidence intervals close to 3%). Low OE infection levels are likely due to low densities of monarchs in this region and/or migratory escape effects, where migrating individuals leave behind areas with high density of conspecifics and high potential for parasite accumulation and transmission. Future work should aim to disentangle the relative contribution of these two mechanisms for governing the decrease in parasitism at the range limits of migratory populations.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

Variability in plant nutrients reduces insect herbivore performance.

The performance and population dynamics of insect herbivores depend on the nutritive and defensive traits of their host plants. The literature on plant-herbivore interactions focuses on plant trait mean values, but recent studies showing the importance of plant genetic diversity for herbivores suggest that plant trait variance may be equally important. The consequences of plant trait variance for herbivore performance, however, have been largely overlooked. Here we report an extensive assessment of the effects of within-population plant trait variance on herbivore performance using 457 performance datasets from 53 species of insect herbivores. We show that variance in plant nutritive traits substantially reduces mean herbivore performance via non-linear averaging of performance relationships that were overwhelmingly concave down. By contrast, relationships between herbivore performance and plant defence levels were typically linear, with variance in plant defence not affecting herbivore performance via non-linear averaging. Our results demonstrate that plants contribute to the suppression of herbivore populations through variable nutrient levels, not just by having low average quality as is typically thought. We propose that this phenomenon could play a key role in the suppression of herbivore populations in natural systems, and that increased nutrient heterogeneity within agricultural crops could contribute to the sustainable control of insect pests in agroecosystems