Shifting the paradigm: The role of introduced plants in the resiliency of terrestrial ecosystems to climate change.

Current ecological communities are in a constant state of flux from climate change and from species introductions. Recent discussion has focused on the positive roles introduced species can play in ecological communities and on the importance of conserving resilient ecosystems, but not how these two ideas intersect. There has been insufficient work to define the attributes needed to support ecosystem resilience to climate change in modern communities. Here, I argue that non-invasive, introduced plant species could play an important role in supporting the resilience of terrestrial ecosystems to climate change. Using examples from multiple taxonomic groups and ecosystems, I discuss how introduced plants can contribute to ecosystem resilience via their roles in plant and insect communities, as well as their associated ecosystem functions. I highlight the current and potential contributions of introduced plants and where there are critical knowledge gaps. Determining when and how introduced plants are contributing to the resilience of ecosystems to climate change will contribute to effective conservation strategies.

Forecasting species' responses to climate change using space-for-time substitution.

To anticipate species' responses to climate change, ecologists have largely relied on the space-for-time-substitution (SFTS) approach. However, the hypothesis and its underlying assumptions have been poorly tested. Here, we detail how the efficacy of using the SFTS approach to predict future locations will depend on species' traits, the ecological context, and whether the species is declining or introduced. We argue that the SFTS approach will be least predictive in the contexts where we most need it to be: forecasting the expansion of the range of introduced species and the recovery of threatened species. We highlight how evaluating the underlying assumptions, along with improved methods, will rapidly advance our understanding of the applicability of the SFTS approach, particularly in the context of modelling the distribution of species.

Lack of evidence for the match-mismatch hypothesis across terrestrial trophic interactions.

Climate change has led to widespread shifts in the timing of key life history events between interacting species (phenological asynchrony) with hypothesized cascading negative fitness impacts on one or more of the interacting species-often termed 'mismatch'. Yet, predicting the types of systems prone to mismatch remains a major hurdle. Recent reviews have argued that many studies do not provide strong evidence of the underlying match-mismatch hypothesis, but none have quantitatively analysed support for it. Here, we test the hypothesis by estimating the prevalence of mismatch across antagonistic trophic interactions in terrestrial systems and then examine whether studies that meet the assumptions of the hypothesis are more likely to find a mismatch. Despite a large range of synchrony to asynchrony, we did not find general support for the hypothesis. Our results thus question the general applicability of this hypothesis in terrestrial systems, but they also suggest specific types of data missing to robustly refute it. We highlight the critical need to define resource seasonality and the window of 'match' for the most rigorous tests of the hypothesis. Such efforts are necessary if we want to predict systems where mismatches are likely to occur.

Flowering phenology influences butterfly nectar foraging on non-native plants in an oak savanna.

The negative impacts of non-native species have been well documented, but some non-natives can play a positive role in native ecosystems. One way that non-native plants can positively interact with native butterflies is by provisioning nectar. Relatively little is known about the role of phenology in determining native butterfly visitation to non-native plants for nectar, yet flowering time directly controls nectar availability. Here we investigate the phenological patterns of flowering by native and non-native plants and nectar foraging by native butterflies in an oak savanna on Vancouver Island, British Columbia, Canada. We also test whether native butterflies select nectar sources in proportion to their availability. We found that non-native plants were well integrated into butterfly nectar diets (83% of foraging observations) and that visitation to non-natives increased later in the season when native plants were no longer flowering. We also found that butterflies selected non-native flowers more often than expected based on their availability, suggesting that these plants represent a potentially valuable resource. Our study shows that non-native species have the potential to drive key species interactions in seasonal ecosystems. Management regimes focused on eradicating non-native species may need to reconsider their aims and evaluate resources that non-natives provide.

Eastern monarch larval performance may not be affected by shifts in phenological synchrony with milkweed.

Interacting species are experiencing disruptions in the relative timing of their key life-history events due to climate change. These shifts can sometimes be detrimental to the fitness of the consumer in trophic interactions but not always.The potential consequences of phenological asynchrony for the monarch butterfly (Danaus plexippus) and its host plant (Asclepias spp.) have not been well-studied. Given that plants generally undergo seasonal declines in quality, if climate change delays the timing of the larval stage relative to the availability of younger milkweed plants, monarch performance could be negatively affected.Here, we explore the potential consequences for the eastern monarch population due to probable asynchrony with milkweed. We used field surveys around Ottawa, Canada, to determine monarch oviposition preference on common milkweed (Asclepias syriaca) plants and the seasonal availability of these plants. To determine the potential fitness consequences when females oviposit on nonpreferred plants, we conducted a field experiment to assess the effect of milkweed size on monarch larval performance (e.g., development time and final size).Preferred oviposition plants (earlier stages of development and better condition) were consistently available in large proportion over the summer season. We also found that declines in leaf quality (more latex and thicker leaves) with plant size did not translate into decreases in larval performance.Our results suggest that even if asynchrony of the monarch-milkweed interaction occurs due to climate change, the larval stage of the eastern monarch may not face negative consequences. Future studies should determine how the relative timing of the interaction will change in the region.

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

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.

Do traits of plant species predict the efficacy of species distribution models for finding new occurrences?

Species distribution models (SDMs) are used to test ecological theory and to direct targeted surveys for species of conservation concern. Several studies have tested for an influence of species traits on the predictive accuracy of SDMs. However, most used the same set of environmental predictors for all species and/or did not use truly independent data to test SDM accuracy. We built eight SDMs for each of 24 plant species of conservation concern, varying the environmental predictors included in each SDM version. We then measured the accuracy of each SDM using independent presence and absence data to calculate area under the receiver operating characteristic curve (AUC) and true positive rate (TPR). We used generalized linear mixed models to test for a relationship between species traits and SDM accuracy, while accounting for variation in SDM performance that might be introduced by different predictor sets. All traits affected one or both SDM accuracy measures. Species with lighter seeds, animal-dispersed seeds, and a higher density of occurrences had higher AUC and TPR than other species, all else being equal. Long-lived woody species had higher AUC than herbaceous species, but lower TPR. These results support the hypothesis that the strength of species-environment correlations is affected by characteristics of species or their geographic distributions. However, because each species has multiple traits, and because AUC and TPR can be affected differently, there is no straightforward way to determine a priori which species will yield useful SDMs based on their traits. Most species yielded at least one useful SDM. Therefore, it is worthwhile to build and test SDMs for the purpose of finding new populations of plant species of conservation concern, regardless of these species' traits.

Patterns and biases in an Arctic herbarium specimen collection: Implications for phenological research.

PREMISE OF THE STUDY: Herbarium specimens are increasingly used in phenological studies. However, natural history collections can have biases that influence the analysis of phenological events. Arctic environments, where remoteness and cold climate govern collection logistics, may give rise to unique or pronounced biases. METHODS: We assessed the presence of biases in time, space, phenological events, collectors, taxonomy, and plant traits across Nunavut using herbarium specimens accessioned at the National Herbarium of Canada (CAN). RESULTS: We found periods of high and low collection that corresponded to societal and institutional events; greater collection density close to common points of air and sea access; and preferences to collect plants at the flowering phase and in peak flower, and to collect particular taxa, flower colours, growth forms, and plant heights. One-quarter of collectors contributed 90% of the collection. DISCUSSION: Collections influenced by temporal and spatial biases have the potential to misrepresent phenology across space and time, whereas those shaped by the interests of collectors or the tendency to favour particular phenological stages, taxa, and plant traits could give rise to imbalanced phenological comparisons. Underlying collection patterns may vary among regions and institutions. To guide phenological analyses, we recommend routine assessment of any herbarium data set prior to its use.

Using insect natural history collections to study global change impacts: challenges and opportunities.

Over the past two decades, natural history collections (NHCs) have played an increasingly prominent role in global change research, but they have still greater potential, especially for the most diverse group of animals on Earth: insects. Here, we review the role of NHCs in advancing our understanding of the ecological and evolutionary responses of insects to recent global changes. Insect NHCs have helped document changes in insects' geographical distributions, phenology, phenotypic and genotypic traits over time periods up to a century. Recent work demonstrates the enormous potential of NHCs data for examining insect responses at multiple temporal, spatial and phylogenetic scales. Moving forward, insect NHCs offer unique opportunities to examine the morphological, chemical and genomic information in each specimen, thus advancing our understanding of the processes underlying species' ecological and evolutionary responses to rapid, widespread global changes.This article is part of the theme issue 'Biological collections for understanding biodiversity in the anthropocene'.

Global shifts in the phenological synchrony of species interactions over recent decades.

Phenological responses to climate change (e.g., earlier leaf-out or egg hatch date) are now well documented and clearly linked to rising temperatures in recent decades. Such shifts in the phenologies of interacting species may lead to shifts in their synchrony, with cascading community and ecosystem consequences. To date, single-system studies have provided no clear picture, either finding synchrony shifts may be extremely prevalent [Mayor SJ, et al. (2017) Sci Rep 7:1902] or relatively uncommon [Iler AM, et al. (2013) Glob Chang Biol 19:2348-2359], suggesting that shifts toward asynchrony may be infrequent. A meta-analytic approach would provide insights into global trends and how they are linked to climate change. We compared phenological shifts among pairwise species interactions (e.g., predator-prey) using published long-term time-series data of phenological events from aquatic and terrestrial ecosystems across four continents since 1951 to determine whether recent climate change has led to overall shifts in synchrony. We show that the relative timing of key life cycle events of interacting species has changed significantly over the past 35 years. Further, by comparing the period before major climate change (pre-1980s) and after, we show that estimated changes in phenology and synchrony are greater in recent decades. However, there has been no consistent trend in the direction of these changes. Our findings show that there have been shifts in the timing of interacting species in recent decades; the next challenges are to improve our ability to predict the direction of change and understand the full consequences for communities and ecosystems.

Insect Development, Thermal Plasticity and Fitness Implications in Changing, Seasonal Environments.

Historical data show that recent climate change has caused advances in seasonal timing (phenology) in many animals and plants, particularly in temperate and higher latitude regions. The population and fitness consequences of these phenological shifts for insects and other ectotherms have been heterogeneous: warming can increase development rates and the number of generations per year (increasing fitness), but can also lead to seasonal mismatches between animals and their resources and increase exposure to environmental variability (decreasing fitness). Insect populations exhibit local adaptation in their developmental responses to temperature, including lower developmental thresholds and the thermal requirements to complete development, but climate change can potentially disrupt seasonal timing of juvenile and adult stages and alter population fitness. We investigate these issues using a global dataset describing how insect developmental responds to temperature via two traits: lower temperature thresholds for development (T0) and the cumulative degree-days required to complete development (G). As suggested by previous analyses, T0 decreases and G increases with increasing (absolute) latitude; however, these traits and the relationship between G and latitude varies significantly among taxonomic orders. The mean number of generations per year (a metric of fitness) increases with both decreasing T0 and G, but the effects of these traits on fitness vary strongly with latitude, with stronger selection on both traits at higher (absolute) latitudes. We then use the traits to predict developmental timing and temperatures for multiple generations within seasons and across years (1970-2010). Seasonality drives developmental temperatures to peak mid-season and for generation lengths to decline across seasons, particularly in temperate regions. We predict that climate warming has advanced phenology and increased the number of generations, particularly at high latitudes. The magnitude of increases in developmental temperature varies little across latitude. Increases in the number of seasonal generations have been greatest for populations experiencing the greatest phenological advancements and warming. Shifts in developmental rate and timing due to climate change will have complex implications for selection and fitness in seasonal environments.

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.

A synthesis of transplant experiments and ecological niche models suggests that range limits are often niche limits.

Global change has made it important to understand the factors that shape species' distributions. Central to this area of research is the question of whether species' range limits primarily reflect the distribution of suitable habitat (i.e. niche limits) or arise as a result of dispersal limitation. Over-the-edge transplant experiments and ecological niche models are commonly used to address this question, yet few studies have taken advantage of a combined approach for inferring the causes of range limits. Here, we synthesise results from existing transplant experiments with new information on the predicted suitability of sites based on niche models. We found that individual performance and habitat suitability independently decline beyond range limits across multiple species. Furthermore, inferences from transplant experiments and niche models were generally concordant within species, with 31 out of 40 cases fully supporting the hypothesis that range limits are niche limits. These results suggest that range limits are often niche limits and that the factors constraining species' ranges operate at scales detectable by both transplant experiments and niche models. In light of these findings, we outline an integrative framework for addressing the causes of range limits in individual species.

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. 5. 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.

The effects of experimental warming on the timing of a plant-insect herbivore interaction.

The phenology of many species is shifting in response to climatic changes, and these shifts are occurring at varying rates across species. This can potentially affect species' interactions and individual fitness. However, few studies have experimentally tested the influence of warming on the timing of species interactions. This is an important gap in the literature given the potential for different direct and indirect effects of temperature via phenological change. Our aim was to test the effects of warming on the western tent caterpillar (Malacosoma californicum pluviale). In addition to the direct effects of warming, we considered the two primary indirect effects mediated by warming-driven changes in its host plant, red alder (Alnus rubra): changes in resource availability due to phenological mismatch (i.e. changes in the relative timing of the interaction), and changes in resource quality associated with leaf maturation. We experimentally warmed egg masses and larvae of the western tent caterpillar placed on branches of red alder in the field. Warming advanced the timing of larval but not leaf emergence. This led to varying degrees of phenological mismatch, with larvae emerging as much as 25 days before to 10 days after the emergence of leaves. Even the earliest-emerging larvae, however, had high survival in the absence of leaves for up to 3 weeks, and they were surprisingly resistant to starvation. In addition, although warming created phenological mismatch that initially slowed the development of larvae that emerged before leaf emergence, it accelerated larval development once leaves were available. Therefore, warming had no net effect on our measures of insect performance. Our results demonstrate that the indirect effects of warming, in creating phenological mismatch, are as important to consider as the direct effects on insect performance. Although future climatic warming might influence plants and insects in different ways, some insects may be well adapted to variation in the timing of their interactions.

A bioenergetic framework for the temperature dependence of trophic interactions.

Changing temperature can substantially shift ecological communities by altering the strength and stability of trophic interactions. Because many ecological rates are constrained by temperature, new approaches are required to understand how simultaneous changes in multiple rates alter the relative performance of species and their trophic interactions. We develop an energetic approach to identify the relationship between biomass fluxes and standing biomass across trophic levels. Our approach links ecological rates and trophic dynamics to measure temperature-dependent changes to the strength of trophic interactions and determine how these changes alter food web stability. It accomplishes this by using biomass as a common energetic currency and isolating three temperature-dependent processes that are common to all consumer-resource interactions: biomass accumulation of the resource, resource consumption and consumer mortality. Using this framework, we clarify when and how temperature alters consumer to resource biomass ratios, equilibrium resilience, consumer variability, extinction risk and transient vs. equilibrium dynamics. Finally, we characterise key asymmetries in species responses to temperature that produce these distinct dynamic behaviours and identify when they are likely to emerge. Overall, our framework provides a mechanistic and more unified understanding of the temperature dependence of trophic dynamics in terms of ecological rates, biomass ratios and stability.

Predicting the sensitivity of butterfly phenology to temperature over the past century.

Studies to date have documented substantial variation among species in the degree to which phenology responds to temperature and shifts over time, but we have a limited understanding of the causes of such variation. Here, we use a spatially and temporally extensive data set (ca. 48 000 observations from across Canada) to evaluate the utility of museum collection records in detecting broad-scale phenology-temperature relationships and to test for systematic differences in the sensitivity of phenology to temperature (days °C(-1) ) of Canadian butterfly species according to relevant ecological traits. We showed that the timing of flight season predictably responded to temperature both across space (variation in average temperature from site to site in Canada) and across time (variation from year to year within each individual site). This reveals that collection records, a vastly underexploited resource, can be applied to the quantification of broad-scale relationships between species' phenology and temperature. The timing of the flight season of earlier fliers and less mobile species was more sensitive to temperature than later fliers and more mobile species, demonstrating that ecological traits can account for some of the interspecific variation in species' phenological sensitivity to temperature. Finally, we found that phenological sensitivity to temperature differed across time and space implying that both dimensions of temperature will be needed to translate species' phenological sensitivity to temperature into accurate predictions of species' future phenological shifts. Given the widespread temperature sensitivity of flight season timing, we can expect long-term temporal shifts with increased warming [ca. 2.4 days °C(-1) (0.18 SE)] for many if not most butterfly species.

Historical ecology: using unconventional data sources to test for effects of global environmental change.

Predicting the future ecological impact of global change drivers requires understanding how these same drivers have acted in the past to produce the plant populations and communities we see today. Historical ecological data sources have made contributions of central importance to global change biology, but remain outside the toolkit of most ecologists. Here we review the strengths and weaknesses of four unconventional sources of historical ecological data: land survey records, "legacy" vegetation data, historical maps and photographs, and herbarium specimens. We discuss recent contributions made using these data sources to understanding the impacts of habitat disturbance and climate change on plant populations and communities, and the duration of extinction-colonization time lags in response to landscape change. Historical data frequently support inferences made using conventional ecological studies (e.g., increases in warm-adapted species as temperature rises), but there are cases when the addition of different data sources leads to different conclusions (e.g., temporal vegetation change not as predicted by chronosequence studies). The explicit combination of historical and contemporary data sources is an especially powerful approach for unraveling long-term consequences of multiple drivers of global change. Despite the limitations of historical data, which include spotty and potentially biased spatial and temporal coverage, they often represent the only means of characterizing ecological phenomena in the past and have proven indispensable for characterizing the nature, magnitude, and generality of global change impacts on plant populations and communities.

Tent caterpillars are robust to variation in leaf phenology and quality in two thermal environments.

The synchrony between emergence of spring-active, insect herbivores and the budburst of their host plants could be affected by warming temperatures with influences on the availability and quality of foliage as it undergoes physical and chemical changes. This can affect the growth and survival of insects. Here, we used sun-exposed and shaded trees to determine whether the synchrony between egg hatch of western tent caterpillar, Malacosoma californicum pluviale Dyar (Lepidoptera:Lasiocampidae) and budburst of its host red alder, Alnus rubra Bongard (Betulaceae)changes with different thermal environments (temperature and light together). To explore the potential outcome of a shift in phenological synchrony, we used laboratory assays of larval growth and survival to determine the effect of variation in young, youthful and mature leaves from sun-exposed and shaded trees. While the average higher temperature of sun-exposed trees advanced the timing of budburst and egg hatch, synchrony was not disrupted. Leaf quality had no significant influence on growth or survival in the laboratory for early instars reared as family groups. Later instar larvae, however, performed best on mature leaves from sun-exposed trees. The robust relationship between leaf and larval development of western tent caterpillars suggests that warming climates may not have a strong negative impact on their success through shifts in phenological synchrony, but might influence other aspects of leaf quality and larval condition.

Historically calibrated predictions of butterfly species' range shift using global change as a pseudo-experiment.

Global changes have the potential to cause a mass extinction. Predicting how species will respond to anticipated changes is a necessary prerequisite to effectively conserving them and reducing extinction rates. Species niche models are widely used for such predictions, but their reliability over long time periods is known to vary. However, climate and land use changes in northern countries provide a pseudo-experiment to test model reliability for predicting future conditions, provided historical data on both species distributions and environmental conditions are available. Using maximum entropy, a prominent modeling technique, we constructed historical models of butterfly species' ranges across Canada and then ran the models forward to present-day to test how well they predicted the current ranges of species. For the majority of species, projections of how we predicted species would respond to known climate changes corresponded with species' observed responses (mean autoregressive R2 = 0.70). This correspondence declined for northerly and very widely distributed species. Our results demonstrate that at least some species are tracking shifting climatic conditions across very large geographic areas and that these shifts can be predicted accurately using niche models. We also found, however, that models for some species fail when projected through time despite high spatial model accuracies during model training, highlighting the need to base management decisions on species assemblages, not individual species.