Thirty-six years of butterfly monitoring, snow cover, and plant productivity reveal negative impacts of warmer winters and increased productivity on montane species.

Climate change is contributing to declines of insects through rising temperatures, altered precipitation patterns, and an increasing frequency of extreme events. The impacts of both gradual and sudden shifts in weather patterns are realized directly on insect physiology and indirectly through impacts on other trophic levels. Here, we investigated direct effects of seasonal weather on butterfly occurrences and indirect effects mediated by plant productivity using a temporally intensive butterfly monitoring dataset, in combination with high-resolution climate data and a remotely sensed indicator of plant primary productivity. Specifically, we used Bayesian hierarchical path analysis to quantify relationships between weather and weather-driven plant productivity on the occurrence of 94 butterfly species from three localities distributed across an elevational gradient. We found that snow pack exerted a strong direct positive effect on butterfly occurrence and that low snow pack was the primary driver of reductions during drought. Additionally, we found that plant primary productivity had a consistently negative effect on butterfly occurrence. These results highlight mechanisms of weather-driven declines in insect populations and the nuances of climate change effects involving snow melt, which have implications for ecological theories linking topographic complexity to ecological resilience in montane systems.

Insects and recent climate change.

Insects have diversified through more than 450 million y of Earth's changeable climate, yet rapidly shifting patterns of temperature and precipitation now pose novel challenges as they combine with decades of other anthropogenic stressors including the conversion and degradation of land. Here, we consider how insects are responding to recent climate change while summarizing the literature on long-term monitoring of insect populations in the context of climatic fluctuations. Results to date suggest that climate change impacts on insects have the potential to be considerable, even when compared with changes in land use. The importance of climate is illustrated with a case study from the butterflies of Northern California, where we find that population declines have been severe in high-elevation areas removed from the most immediate effects of habitat loss. These results shed light on the complexity of montane-adapted insects responding to changing abiotic conditions. We also consider methodological issues that would improve syntheses of results across long-term insect datasets and highlight directions for future empirical work.

Extreme heterogeneity of population response to climatic variation and the limits of prediction.

Certain general facets of biotic response to climate change, such as shifts in phenology and geographic distribution, are well characterized; however, it is not clear whether the observed similarity of responses across taxa will extend to variation in other population-level processes. We examined population response to climatic variation using long-term incidence data (collected over 42 years) encompassing 149 butterfly species and considerable habitat diversity (10 sites along an elevational gradient from sea level to over 2,700 m in California). Population responses were characterized by extreme heterogeneity that was not attributable to differences in species composition among sites. These results indicate that habitat heterogeneity might be a buffer against climate change and highlight important questions about mechanisms maintaining interpopulation differences in responses to weather. Despite overall heterogeneity of response, population dynamics were accurately predicted by our model for many species at each site. However, the overall correlation between observed and predicted incidence in a cross validation analysis was moderate (Pearson's r = 0.23, SE 0.01), and 97% of observed data fell within the predicted 95% credible intervals. Prediction was most successful for more abundant species as well as for sites with lower annual turnover. Population-level heterogeneity in response to climate variation and the limits of our predictive power highlight the challenges for a future of increasing climatic variability.

Synchronous population dynamics in California butterflies explained by climatic forcing.

A long-standing challenge for population biology has been to understand why some species are characterized by populations that fluctuate in size independently, while populations of other species fluctuate synchronously across space. The effects of climatic variation and dispersal have been invoked to explain synchronous population dynamics, however an understanding of the relative influence of these drivers in natural populations is lacking. Here we compare support for dispersal- versus climate-driven models of interspecific variation in synchrony using 27 years of observations of 65 butterfly species at 10 sites spanning 2750 m of elevation in Northern California. The degree of spatial synchrony exhibited by each butterfly species was used as a response in a unique approach that allowed us to investigate whether interspecific variation in response to climate or dispersal propensity was most predictive of interspecific variation in synchrony. We report that variation in sensitivity to climate explained 50% of interspecific variation in synchrony, whereas variation in dispersal propensity explained 23%. Sensitivity to the El Niño Southern Oscillation, a primary driver of regional climate, was the best predictor of synchrony. Combining sensitivity to climate and dispersal propensity into a single model did not greatly increase model performance, confirming the primacy of climatic sensitivity for driving spatial synchrony in butterflies. Finally, we uncovered a relationship between spatial synchrony and population decline that is consistent with theory, but small in magnitude, which suggests that the degree to which populations fluctuate in synchrony is of limited use for understanding the ongoing decline of the Northern California butterfly fauna.

Sympatric, temporally isolated populations of the pine white butterfly Neophasia menapia, are morphologically and genetically differentiated.

Temporal isolation remains an understudied, and potentially under-appreciated, mechanism of reproductive isolation. Phenological differences have been discovered in populations of the pine white butterfly (Neophasia menapia), a typically univoltine species found throughout western North America. At two locations in the Coast Range of California there are two periods of adult emergence per year, one in early summer (July) and one in late summer/autumn (September/October). Differences in flight time are accompanied by differences in wing shape and pigmentation. Here we use a combination of population genomics and morphological analyses to assess the extent to which temporal isolation is able to limit gene flow between sympatric early and late flights. Not only did we detect both genetic and morphological differences between early and late flights at the two sites, we also found that the patterns of differentiation between the two flights were different at each location, suggesting an independent origin for the two sympatric flights. Additionally, we found no evidence that these sympatric flights originated via colonization from any of the other sampled localities. We discuss several potential hypotheses about the origin of these temporally isolated sympatric flights.

Increasing neonicotinoid use and the declining butterfly fauna of lowland California.

The butterfly fauna of lowland Northern California has exhibited a marked decline in recent years that previous studies have attributed in part to altered climatic conditions and changes in land use. Here, we ask if a shift in insecticide use towards neonicotinoids is associated with butterfly declines at four sites in the region that have been monitored for four decades. A negative association between butterfly populations and increasing neonicotinoid application is detectable while controlling for land use and other factors, and appears to be more severe for smaller-bodied species. These results suggest that neonicotinoids could influence non-target insect populations occurring in proximity to application locations, and highlights the need for mechanistic work to complement long-term observational data.

Midpoint attractors and species richness: Modelling the interaction between environmental drivers and geometric constraints.

We introduce a novel framework for conceptualising, quantifying and unifying discordant patterns of species richness along geographical gradients. While not itself explicitly mechanistic, this approach offers a path towards understanding mechanisms. In this study, we focused on the diverse patterns of species richness on mountainsides. We conjectured that elevational range midpoints of species may be drawn towards a single midpoint attractor - a unimodal gradient of environmental favourability. The midpoint attractor interacts with geometric constraints imposed by sea level and the mountaintop to produce taxon-specific patterns of species richness. We developed a Bayesian simulation model to estimate the location and strength of the midpoint attractor from species occurrence data sampled along mountainsides. We also constructed midpoint predictor models to test whether environmental variables could directly account for the observed patterns of species range midpoints. We challenged these models with 16 elevational data sets, comprising 4500 species of insects, vertebrates and plants. The midpoint predictor models generally failed to predict the pattern of species midpoints. In contrast, the midpoint attractor model closely reproduced empirical spatial patterns of species richness and range midpoints. Gradients of environmental favourability, subject to geometric constraints, may parsimoniously account for elevational and other patterns of species richness.

Understanding a migratory species in a changing world: climatic effects and demographic declines in the western monarch revealed by four decades of intensive monitoring.

Migratory animals pose unique challenges for conservation biologists, and we have much to learn about how migratory species respond to drivers of global change. Research has cast doubt on the stability of the eastern monarch butterfly (Danaus plexippus) population in North America, but the western monarchs have not been as intensively examined. Using a Bayesian hierarchical model, sightings of western monarchs over approximately 40 years were investigated using summer flight records from ten sites along an elevational transect in Northern California. Multiple weather variables were examined, including local and regional temperature and precipitation. Population trends from the ten focal sites and a subset of western overwintering sites were compared to summer and overwintering data from the eastern migration. Records showed western overwintering grounds and western breeding grounds had negative trends over time, with declines concentrated early in the breeding season, which were potentially more severe than in the eastern population. Temporal variation in the western monarch also appears to be largely independent of (uncorrelated with) the dynamics in the east. For our focal sites, warmer temperatures had positive effects during winter and spring, and precipitation had a positive effect during spring. These climatic associations add to our understanding of biotic-abiotic interactions in a migratory butterfly, but shifting climatic conditions do not explain the overall, long-term, negative population trajectory observed in our data.

Molecular evidence for hybridization in Colias (Lepidoptera: Pieridae): are Colias hybrids really hybrids?

Gene flow and hybridization among species dramatically affect our understanding of the species as a biological unit, species relationships, and species adaptations. In North American Colias eurytheme and Colias eriphyle, there has been historical debate over the extent of hybridization occurring and the identity of phenotypically intermediate individuals as genetic hybrids. This study assesses the population structure of these two species to measure the extent of hybridization and the genetic identity of phenotypic intermediates as hybrids. Amplified fragment length polymorphism (AFLP) marker analysis was performed on 378 specimens collected from northern California and Nevada. Population structure was inferred using a Bayesian/Markov chain Monte Carlo method, which probabilistically assigns individuals to genetic clusters. Three genetic clusters provided the best fit for the data. C. eurytheme individuals were primarily assigned to two closely related clusters, and C. eriphyle individuals were mostly assigned to a third, more distantly related cluster. There appeared to be significant hybridization between the two species. Individuals of intermediate phenotype (putative hybrids) were found to be genetically indistinguishable from C. eriphyle, indicating that previous work based on the assumption that these intermediate forms are hybrids may warrant reconsideration.

Species with more volatile population dynamics are differentially impacted by weather.

Climatic variation has been invoked as an explanation of population dynamics for a variety of taxa. Much work investigating the link between climatic forcings and population fluctuation uses single-taxon case studies. Here, we conduct comparative analyses of a multi-decadal dataset describing population dynamics of 50 co-occurring butterfly species at 10 sites in Northern California. Specifically, we explore the potential commonality of response to weather among species that encompass a gradient of population dynamics via a hierarchical Bayesian modelling framework. Results of this analysis demonstrate that certain weather conditions impact volatile, or irruptive, species differently as compared with relatively stable species. Notably, precipitation-related variables, including indices of the El Niño Southern Oscillation, have a more pronounced impact on the most volatile species. We hypothesize that these variables influence vegetation resource availability, and thus indirectly influence population dynamics of volatile taxa. As one of the first studies to show a common influence of weather among taxa with similar population dynamics, the results presented here suggest new lines of research in the field of biotic-abiotic interactions.

Global weather and local butterflies: variable responses to a large-scale climate pattern along an elevational gradient.

Understanding the spatial and temporal scales at which environmental variation affects populations of plants and animals is an important goal for modern population biology, especially in the context of shifting climatic conditions. The El Niño Southern Oscillation (ENSO) generates climatic extremes of interannual variation, and has been shown to have significant effects on the diversity and abundance of a variety of terrestrial taxa. However, studies that have investigated the influence of such large-scale climate phenomena have often been limited in spatial and taxonomic scope. We used 23 years (1988-2010) of a long-term butterfly monitoring data set to explore associations between variation in population abundance of 28 butterfly species and variation in ENSO-derived sea surface temperature anomalies (SSTA) across 10 sites that encompass an elevational range of 2750 m in the Sierra Nevada mountain range of California. Our analysis detected a positive, regional effect of increased SSTA on butterfly abundance (wetter and warmer years predict more butterfly observations), yet the influence of SSTA on butterfly abundances varied along the elevational gradient, and also differed greatly among the 28 species. Migratory species had the strongest relationships with ENSO-derived SSTA, suggesting that large-scale climate indices are particularly valuable for understanding biotic-abiotic relationships of the most mobile species. In general, however, the ecological effects of large-scale climatic factors are context dependent between sites and species. Our results illustrate the power of long-term data sets for revealing pervasive yet subtle climatic effects, but also caution against expectations derived from exemplar species or single locations in the study of biotic-abiotic interactions.

Variation in wing pattern and palatability in a female-limited polymorphic mimicry system.

Checkerspot butterflies in the genera Euphydryas and Chlosyne exhibit phenotypic polymorphisms along a well-defined latitudinal and elevational gradient in California. The patterns of phenotypic variation in Euphydryas chalcedona, Chlosyne palla, and Chlosyne hoffmanni suggest a mimetic relationship; in addition, the specific patterns of variation in C. palla suggest a female-limited polymorphic mimicry system (FPM). However, the existence of polymorphic models runs counter to predictions of mimicry theory. Palatability trials were undertaken to assess whether or not the different color morphs of each species were distasteful or toxic to a generalized avian predator, the European starling (Sturnus vulgaris). Results indicate that the black morph of E. chalcedona is distasteful, but not toxic, to predators, while the red morph is palatable. C . hoffmanni and both color morphs of C. palla are palatable to predators. Predators that learn to reject black E. chalcedona also reject black C. palla, suggesting that the latter is a FPM of the former. C. hoffmanni does not appear to be involved in this mimetic relationship.

A hierarchical perspective on the diversity of butterfly species' responses to weather in the Sierra Nevada Mountains.

An important and largely unaddressed issue in studies of biotic-abiotic relationships is the extent to which closely related species, or species living in similar habitats, have similar responses to weather. We addressed this by applying a hierarchical, Bayesian analytical framework to a long-term data set for butterflies which allowed us to simultaneously investigate responses of the entire fauna and individual species. A small number of variables had community-level effects. In particular, higher total annual snow depth had a positive effect on butterfly occurrences, while spring minimum temperature and El Niño-Southern Oscillation (ENSO) sea-surface variables for April-May had negative standardized coefficients. Our most important finding was that variables with large impacts at the community-level did not necessarily have a consistent response across all species. Species-level responses were much more similar to each other for snow depth compared to the other variables with strong community effects. This variation in species-level responses to weather variables raises important complications for the prediction of biotic responses to shifting climatic conditions. In addition, we found that clear associations with weather can be detected when considering ecologically delimited subsets of the community. For example, resident species and non-ruderal species had a much more unified response to weather variables compared to non-resident species and ruderal species, which suggests local adaptation to climate. These results highlight the complexity of biotic-abiotic interactions and confront that complexity with methodological advances that allow ecologists to understand communities and shifting climates while simultaneously revealing species-specific variation in response to climate.

A time-calibrated phylogeny of the butterfly tribe Melitaeini.

The butterfly tribe Melitaeini [Nymphalidae] contains numerous species that have been the subjects of a wide range of biological studies. Despite numerous taxonomic revisions, many of the evolutionary relationships within the tribe remain unresolved. Utilizing mitochondrial and nuclear gene regions, we produced a time-calibrated phylogenetic hypothesis for 222 exemplars comprising at least 178 different species and 21 of the 22 described genera, making this the most complete phylogeny of the tribe to date. Our results suggest that four well-supported clades corresponding to the subtribes Euphydryina, Chlosynina, Melitaeina, and Phyciodina exist within the tribe. This analysis is also represents the most complete phylogenetic analysis of the Chlosynina to date, and includes several genera and species that have been previously excluded from published phylogenies of this group.

Contribution of urban expansion and a changing climate to decline of a butterfly fauna.

Butterfly populations are naturally patchy and undergo extinctions and recolonizations. Analyses based on more than 2 decades of data on California's Central Valley butterfly fauna show a net loss in species richness through time. We analyzed 22 years of phenological and faunistic data for butterflies to investigate patterns of species richness over time. We then used 18-22 years of data on changes in regional land use and 37 years of seasonal climate data to develop an explanatory model. The model related the effects of changes in land-use patterns, from working landscapes (farm and ranchland) to urban and suburban landscapes, and of a changing climate on butterfly species richness. Additionally, we investigated local trends in land use and climate. A decline in the area of farmland and ranchland, an increase in minimum temperatures during the summer and maximum temperatures in the fall negatively affected net species richness, whereas increased minimum temperatures in the spring and greater precipitation in the previous summer positively affected species richness. According to the model, there was a threshold between 30% and 40% working-landscape area below which further loss of working-landscape area had a proportionally greater effect on butterfly richness. Some of the isolated effects of a warming climate acted in opposition to affect butterfly richness. Three of the 4 climate variables that most affected richness showed systematic trends (spring and summer mean minimum and fall mean maximum temperatures). Higher spring minimum temperatures were associated with greater species richness, whereas higher summer temperatures in the previous year and lower rainfall were linked to lower richness. Patterns of land use contributed to declines in species richness (although the pattern was not linear), but the net effect of a changing climate on butterfly richness was more difficult to discern.

Drivers of hybridization in a 66-generation record of Colias butterflies.

Hybridization significantly affects the ecology and evolution of numerous plant and animal lineages. Most studies have focused on endogenous drivers of hybridization and neglected variation in exogenous factors, such as seasonal weather patterns. In this study, we take advantage of a unique dataset consisting of records of hybridization between the butterflies Colias eurytheme and C. eriphyle (Pieridae) for 66 generations (22 years) to investigate the importance of seasonal weather on the production and survival of hybrid offspring. Important seasonal weather variables for each parental species and hybrid offspring were determined using model averaging, and these weather variables, along with butterfly abundances, were analyzed using path analysis. The most important drivers of hybridization were the abundance of C. eriphyle, summer minimum temperature, and spring maximum temperature. In contrast, the abundance of C. eurytheme and weather variables prior to the current flight season were relatively unimportant for variation in hybrid abundance. Parental abundances were mostly driven by weather variables prior to the flight season possibly because these variables affect host plant quality. Our results suggest that exogenous, climatic factors can influence hybridization in natural systems, and that these factors can act both directly on hybrid abundance and indirectly through the population dynamics of parental species.

Use of exotic hosts by Lepidoptera: widespread species colonize more novel hosts.

The study of host shifts by herbivorous insects has played an important role in evolutionary biology, contributing to research in coevolution, ecological speciation, and adaptive radiation. As invasive plants become more abundant in many ecosystems, the potential for exotic host use by native insects increases. Graves and Shapiro (2003) have documented exotic host use by 34% of Californian butterflies, suggesting that the plants and butterflies of California might be an important model system for the colonization and utilization of novel resources. In this study, we analyze relationships among geographic range, native diet breadth, and the use of exotic hosts by Californian butterflies and skippers (Lepidoptera). Geographic range and, to a lesser extent, native diet breadth are significant predictors of exotic host use, with positive relationships found both before and after phylogenetic correction. These results give insight into the process of insect host range evolution, as geographically widespread generalists have an apparently greater tendency to use novel, exotic hosts than geographically constrained specialists. Increasing occurrences of exotic host use are expected and those species not capable of shifting to nonnative hosts are likely to have higher vulnerability to extirpation and extinction in the future.

The race is not to the swift: long-term data reveal pervasive declines in California's low-elevation butterfly fauna.

Understanding the ecology of extinction is one of the primary challenges facing ecologists in the 21st century. Much of our current understanding of extinction, particularly for invertebrates, comes from studies with large geographic coverage but less temporal resolution, such as comparisons between historical collection records and contemporary surveys for geographic regions or political entities. We present a complementary approach involving a data set that is geographically restricted but temporally intensive: we focus on three sites in the Central Valley of California, and utilize 35 years of biweekly (every two weeks) surveys at our most long-sampled site. Previous analyses of these data revealed declines in richness over recent decades. Here, we take a more detailed approach to investigate the mode of decline for this fauna. We ask if all species are in decline, or only a subset. We also investigate traits commonly found to be predictors of extinction risk in other studies, such as body size, diet breadth, habitat association, and geographic range. We find that population declines are ubiquitous: the majority of species at our three focal sites (but not at a nearby site at higher elevation) are characterized by reductions in the fraction of days that they are observed per year. These declines are not readily predicted by ecological traits, with the possible exception of ruderal/non-ruderal status. Ruderal species, in slightly less precipitous decline than non-ruderal taxa, are more dispersive and more likely to be associated with disturbed habitats and exotic hosts. We conclude that population declines and extirpation, particularly in regions severely and recently impacted by anthropogenic alteration, might not be as predictable as has been suggested by other studies on the ecology of extinction.

A complete record from colonization to extinction reveals density dependence and the importance of winter conditions for a population of the silvery blue, Glaucopsyche lygdamus.

Butterflies in the family Lycaenidac are often the focus of conservation efforts. However, our understanding of lycaenid population dynamics has been limited to relatively few examples of long-term monitoring data that have been reported. Here, factors associated with population regulation are investigated using a complete record of a single population of the silvery blue, Glaucopsyche lygdamus Doubleday (Lepidoptera: Lycaenidae). Adults of G. lygdamus were first observed in an annual grassland near Davis, California, in 1982 and were last seen in 2003. Relationships between inter-annual variation in abundance and climatic variables were examined, accounting for density dependent effects. Significant effects of both negative density dependence and climatic variation were detected, particularly precipitation and temperature during winter months. Variation in precipitation, the strongest predictor of abundance, was associated directly and positively with butterfly abundance in the same year. Winter temperatures had a negative effect in the same year, but had a lagged, positive effect on abundance in the subsequent year. Mechanistic hypotheses are posed that include climatic effects mediated through both larval and adult plant resources.

Compounded effects of climate change and habitat alteration shift patterns of butterfly diversity.

Climate change and habitat destruction have been linked to global declines in vertebrate biodiversity, including mammals, amphibians, birds, and fishes. However, invertebrates make up the vast majority of global species richness, and the combined effects of climate change and land use on invertebrates remain poorly understood. Here we present 35 years of data on 159 species of butterflies from 10 sites along an elevational gradient spanning 0-2,775 m in a biodiversity hotspot, the Sierra Nevada Mountains of Northern California. Species richness has declined at half of the sites, with the most severe reductions at the lowest elevations, where habitat destruction is greatest. At higher elevations, we observed clear upward shifts in the elevational ranges of species, consistent with the influence of global warming. Taken together, these long-term data reveal the interacting negative effects of human-induced changes on both the climate and habitat available to butterfly species in California. Furthermore, the decline of ruderal, disturbance-associated species indicates that the traditional focus of conservation efforts on more specialized and less dispersive species should be broadened to include entire faunas when estimating and predicting the effects of pervasive stressors.