Combining photoperiod and thermal responses to predict phenological mismatch for introduced insects.

A wide variety of organisms use the regular seasonal changes in photoperiod as a cue to align their life cycles with favorable conditions. Yet the phenological consequences of photoperiodism for organisms exposed to new climates are often overlooked. We present a conceptual approach and phenology model that maps voltinism (generations per year) and the degree of phenological mismatch that can arise when organisms with a short-day diapause response are introduced to new regions or are otherwise exposed to new climates. Our degree-day-based model combines continent-wide spatialized daily climate data, calculated date-specific and latitude-specific day lengths, and experimentally determined developmental responses to both photoperiod and temperature. Using the case of the knotweed psyllid Aphalara itadori, a new biological control agent being introduced from Japan to North America and Europe to control an invasive weed, we show how incorporating a short-day diapause response will result in geographic patterns of attempted voltinism that are strikingly different from the potential number of generations based on degree-days alone. The difference between the attempted and potential generations represents a quantitative measure of phenological mismatch between diapause timing and the end of the growing season. We conclude that insects moved from lower to higher latitudes (or to cooler climates) will tend to diapause too late, potentially resulting in high mortality from inclement weather, and those moved from higher to lower latitude (to warmer climates) may be prone to diapausing too early, therefore not fully exploiting the growing season and/or suffering from insufficient reserves for the longer duration in diapause. Mapped output reveals a central region with good phenology match that shifts north or south depending on the geographic source of the insect and its corresponding critical photoperiod for diapause. These results have direct relevance for efforts to establish populations of classical biocontrol agents. More generally, our approach and model could be applied to a wide variety of photoperiod- and temperature-sensitive organisms that are exposed to changes in climate, including resident and invasive agricultural pests and species of conservation concern.

InsectChange: a global database of temporal changes in insect and arachnid assemblages.

Insects are the most ubiquitous and diverse group of eukaryotic organisms on Earth, forming a crucial link in terrestrial and freshwater food webs. They have recently become the subject of headlines because of observations of dramatic declines in some places. Although there are hundreds of long-term insect monitoring programs, a global database for long-term data on insect assemblages has so far remained unavailable. In order to facilitate synthetic analyses of insect abundance changes, we compiled a database of long-term (≥10 yr) studies of assemblages of insects (many also including arachnids) in the terrestrial and freshwater realms. We searched the scientific literature and public repositories for data on insect and arachnid monitoring using standardized protocols over a time span of 10 yr or longer, with at least two sampling events. We focused on studies that presented or allowed calculation of total community abundance or biomass. We extracted data from tables, figures, and appendices, and, for data sets that provided raw data, we standardized trapping effort over space and time when necessary. For each site, we extracted provenance details (such as country, state, and continent) as well as information on protection status, land use, and climatic details from publicly available GIS sources. In all, the database contains 1,668 plot-level time series sourced from 165 studies with samples collected between 1925 and 2018. Sixteen data sets provided here were previously unpublished. Studies were separated into those collected in the terrestrial realm (103 studies with a total of 1,053 plots) and those collected in the freshwater realm (62 studies with 615 plots). Most studies were from Europe (48%) and North America (29%), with 34% of the plots located in protected areas. The median monitoring time span was 19 yr, with 12 sampling years. The number of individuals was reported in 129 studies, the total biomass was reported in 13 studies, and both abundance and biomass were reported in 23 studies. This data set is published under a CC-BY license, requiring attribution of the data source. Please cite this paper if the data are used in publications, and respect the licenses of the original sources when using (part of) their data as detailed in Metadata S1: Table 1.

Divergence in Photoperiod Responses of a Classical Biological Control Agent, Galerucella calmariensis (Coleoptera: Chrysomelidae), Across a Climatic and Latitudinal Gradient.

A key knowledge gap in classical biological control is to what extent insect agents evolve to novel environments. The introduction of biological control agents to new photoperiod regimes and climates may disrupt the coordination of diapause timing that evolved to the growing season length in the native range. We tested whether populations of Galerucella calmariensis L. have evolved in response to the potential mismatch of their diapause timing since their intentional introduction to the United States from Germany in the 1990s. Populations collected from 39.4° to 48.8° latitude in the western United States were reared in growth chambers to isolate the effects of photoperiod on diapause induction and development time. For all populations, shorter day lengths increased the proportion of beetles that entered diapause instead of reproducing. The critical photoperiods, or the day length at which half of a population diapauses, differed significantly among the sampled populations, generally decreasing at lower latitudes. The latitudinal trend reflects changes in growing season length, which determines the number of generations possible, and in local day lengths, at the time when beetles are sensitive to this cue. Development times were similar across populations, with one exception, and did not vary with photoperiod. These results show that there was sufficient genetic variation from the two German source populations to evolve different photoperiod responses across a range of environmental conditions. This study adds to the examples of rapid evolution of seasonal adaptations in introduced insects.

DDRP: Real-time phenology and climatic suitability modeling of invasive insects.

Rapidly detecting and responding to new invasive species and the spread of those that are already established is essential for reducing their potential threat to food production, the economy, and the environment. We describe a new spatial modeling platform that integrates mapping of phenology and climatic suitability in real-time to provide timely and comprehensive guidance for stakeholders needing to know both where and when invasive insect species could potentially invade the conterminous United States. The Degree-Days, Risk, and Phenological event mapping (DDRP) platform serves as an open-source and relatively easy-to-parameterize decision support tool to help detect new invasive threats, schedule monitoring and management actions, optimize biological control, and predict potential impacts on agricultural production. DDRP uses a process-based modeling approach in which degree-days and temperature stress are calculated daily and accumulate over time to model phenology and climatic suitability, respectively. Outputs include predictions of the number of completed generations, life stages present, dates of phenological events, and climatically suitable areas based on two levels of climate stress. Species parameter values can be derived from laboratory and field studies or estimated through an additional modeling step. DDRP is written entirely in R, making it flexible and extensible, and capitalizes on multiple R packages to generate gridded and graphical outputs. We illustrate the DDRP modeling platform and the process of model parameterization using two invasive insect species as example threats to United States agriculture: the light brown apple moth, Epiphyas postvittana, and the small tomato borer, Neoleucinodes elegantalis. We then discuss example applications of DDRP as a decision support tool, review its potential limitations and sources of model error, and outline some ideas for future improvements to the platform.

Developmental trap or demographic bonanza? Opposing consequences of earlier phenology in a changing climate for a multivoltine butterfly.

A rapidly changing climate has the potential to interfere with the timing of environmental cues that ectothermic organisms rely on to initiate and regulate life history events. Short-lived ectotherms that exhibit plasticity in their life history could increase the number of generations per year under warming climate. If many individuals successfully complete an additional generation, the population experiences an additional opportunity to grow, and a warming climate could lead to a demographic bonanza. However, these plastic responses could become maladaptive in temperate regions, where a warmer climate could trigger a developmental pathway that cannot be completed within the growing season, referred to as a developmental trap. Here we incorporated detailed demography into commonly used photothermal models to evaluate these demographic consequences of phenological shifts due to a warming climate on the formerly widespread, multivoltine butterfly (Pieris oleracea). Using species-specific temperature- and photoperiod-sensitive vital rates, we estimated the number of generations per year and population growth rate over the set of climate conditions experienced during the past 38 years. We predicted that populations in the southern portion of its range have added a fourth generation in recent years, resulting in higher annual population growth rates (demographic bonanzas). We predicted that populations in the Northeast United States have experienced developmental traps, where increases in the thermal window initially caused mortality of the final generation and reduced growth rates. These populations may recover if more growing degree days are added to the year. Our framework for incorporating detailed demography into commonly used photothermal models demonstrates the importance of using both demography and phenology to predict consequences of phenological shifts.

Butterfly abundance declines over 20 years of systematic monitoring in Ohio, USA.

Severe insect declines make headlines, but they are rarely based on systematic monitoring outside of Europe. We estimate the rate of change in total butterfly abundance and the population trends for 81 species using 21 years of systematic monitoring in Ohio, USA. Total abundance is declining at 2% per year, resulting in a cumulative 33% reduction in butterfly abundance. Three times as many species have negative population trends compared to positive trends. The rate of total decline and the proportion of species in decline mirror those documented in three comparable long-term European monitoring programs. Multiple environmental changes such as climate change, habitat degradation, and agricultural practices may contribute to these declines in Ohio and shift the makeup of the butterfly community by benefiting some species over others. Our analysis of life-history traits associated with population trends shows an impact of climate change, as species with northern distributions and fewer annual generations declined more rapidly. However, even common and invasive species associated with human-dominated landscapes are declining, suggesting widespread environmental causes for these trends. Declines in common species, although they may not be close to extinction, will have an outsized impact on the ecosystem services provided by insects. These results from the most extensive, systematic insect monitoring program in North America demonstrate an ongoing defaunation in butterflies that on an annual scale might be imperceptible, but cumulatively has reduced butterfly numbers by a third over 20 years.