Predator mass mortality events restructure food webs through trophic decoupling.

Predators have a key role in structuring ecosystems1-4. However, predator loss is accelerating globally4-6, and predator mass-mortality events7 (MMEs)-rapid large-scale die-offs-are now emblematic of the Anthropocene epoch6. Owing to their rare and unpredictable nature7, we lack an understanding of how MMEs immediately impact ecosystems. Past predator-removal studies2,3 may be insufficient to understand the ecological consequences of MMEs because, in nature, dead predators decompose in situ and generate a resource pulse8, which could alter ensuing ecosystem dynamics by temporarily enhancing productivity. Here we experimentally induce MMEs in tritrophic, freshwater lake food webs and report ecological dynamics that are distinct from predator losses2,3 or resource pulses9 alone, but that can be predicted from theory8. MMEs led to the proliferation of diverse consumer and producer communities resulting from weakened top-down predator control1-3 and stronger bottom-up effects through predator decomposition8. In contrast to predator removals alone, enhanced primary production after MMEs dampened the consumer community response. As a consequence, MMEs generated biomass dynamics that were most similar to those of undisturbed systems, indicating that they may be cryptic disturbances in nature. These biomass dynamics led to trophic decoupling, whereby the indirect beneficial effects of predators on primary producers are lost and later materialize as direct bottom-up effects that stimulate primary production amid intensified herbivory. These results reveal ecological signatures of MMEs and demonstrate the feasibility of forecasting novel ecological dynamics arising with intensifying global change.

Effects of thermal fluctuations on biological processes: a meta-analysis of experiments manipulating thermal variability.

Thermal variability is a key driver of ecological processes, affecting organisms and populations across multiple temporal scales. Despite the ubiquity of variation, biologists lack a quantitative synthesis of the observed ecological consequences of thermal variability across a wide range of taxa, phenotypic traits and experimental designs. Here, we conduct a meta-analysis to investigate how properties of organisms, their experienced thermal regime and whether thermal variability is experienced in either the past (prior to an assay) or present (during the assay) affect performance relative to the performance of organisms experiencing constant thermal environments. Our results-which draw upon 1712 effect sizes from 75 studies-indicate that the effects of thermal variability are not unidirectional and become more negative as mean temperature and fluctuation range increase. Exposure to variation in the past decreases performance to a greater extent than variation experienced in the present and increases the costs to performance more than diminishing benefits across a broad set of empirical studies. Further, we identify life-history attributes that predictably modify the ecological response to variation. Our findings demonstrate that effects of thermal variability on performance are context-dependent, yet negative outcomes may be heightened in warmer, more variable climates.

Opportunities for behavioral rescue under rapid environmental change.

Laboratory measurements of physiological and demographic tolerances are important in understanding the impact of climate change on species diversity; however, it has been recognized that forecasts based solely on these laboratory estimates overestimate risk by omitting the capacity for species to utilize microclimatic variation via behavioral adjustments in activity patterns or habitat choice. The complex, and often context-dependent nature, of microclimate utilization has been an impediment to the advancement of general predictive models. Here, we overcome this impediment and estimate the potential impact of warming on the fitness of ectotherms using a benefit/cost trade-off derived from the simple and broadly documented thermal performance curve and a generalized cost function. Our framework reveals that, for certain environments, the cost of behavioral thermoregulation can be reduced as warming occurs, enabling behavioral buffering (e.g., the capacity for behavior to ameliorate detrimental impacts) and "behavioral rescue" from extinction in extreme cases. By applying our framework to operative temperature and physiological data collected at an extremely fine spatial scale in an African lizard, we show that new behavioral opportunities may emerge. Finally, we explore large-scale geographic differences in the impact of behavior on climate-impact projections using a global dataset of 38 insect species. These multiple lines of inference indicate that understanding the existing relationship between thermal characteristics (e.g., spatial configuration, spatial heterogeneity, and modal temperature) is essential for improving estimates of extinction risk.

Gradual plasticity alters population dynamics in variable environments: thermal acclimation in the green alga Chlamydomonas reinhartdii.

Environmental variability is ubiquitous, but its effects on populations are not fully understood or predictable. Recent attention has focused on how rapid evolution can impact ecological dynamics via adaptive trait change. However, the impact of trait change arising from plastic responses has received less attention, and is often assumed to optimize performance and unfold on a separate, faster timescale than ecological dynamics. Challenging these assumptions, we propose that gradual plasticity is important for ecological dynamics, and present a study of the plastic responses of the freshwater green algae Chlamydomonas reinhardtii as it acclimates to temperature changes. First, we show that C. reinhardtii's gradual acclimation responses can both enhance and suppress its performance after a perturbation, depending on its prior thermal history. Second, we demonstrate that where conventional approaches fail to predict the population dynamics of C. reinhardtii exposed to temperature fluctuations, a new model of gradual acclimation succeeds. Finally, using high-resolution data, we show that phytoplankton in lake ecosystems can experience thermal variation sufficient to make acclimation relevant. These results challenge prevailing assumptions about plasticity's interactions with ecological dynamics. Amidst the current emphasis on rapid evolution, it is critical that we also develop predictive methods accounting for plasticity.

Temporal heterogeneity increases with spatial heterogeneity in ecological communities.

Heterogeneity is increasingly recognized as a foundational characteristic of ecological systems. Under global change, understanding temporal community heterogeneity is necessary for predicting the stability of ecosystem functions and services. Indeed, spatial heterogeneity is commonly used in alternative stable state theory as a predictor of temporal heterogeneity and therefore an early indicator of regime shifts. To evaluate whether spatial heterogeneity in species composition is predictive of temporal heterogeneity in ecological communities, we analyzed 68 community data sets spanning freshwater and terrestrial systems where measures of species abundance were replicated over space and time. Of the 68 data sets, 55 (81%) had a weak to strongly positive relationship between spatial and temporal heterogeneity, while in the remaining communities the relationship was weak to strongly negative (19%). Based on a mixed model analysis, we found a significant but weak overall positive relationship between spatial and temporal heterogeneity across all data sets combined, and within aquatic and terrestrial data sets separately. In addition, lifespan and successional stage were negatively and positively related to temporal heterogeneity, respectively. We conclude that spatial heterogeneity may be a predictor of temporal heterogeneity in ecological communities, and that this relationship may be a general property of many terrestrial and aquatic communities.

Recent shifts in the occurrence, cause, and magnitude of animal mass mortality events.

Mass mortality events (MMEs) are rapidly occurring catastrophic demographic events that punctuate background mortality levels. Individual MMEs are staggering in their observed magnitude: removing more than 90% of a population, resulting in the death of more than a billion individuals, or producing 700 million tons of dead biomass in a single event. Despite extensive documentation of individual MMEs, we have no understanding of the major features characterizing the occurrence and magnitude of MMEs, their causes, or trends through time. Thus, no framework exists for contextualizing MMEs in the wake of ongoing global and regional perturbations to natural systems. Here we present an analysis of 727 published MMEs from across the globe, affecting 2,407 animal populations. We show that the magnitude of MMEs has been intensifying for birds, fishes, and marine invertebrates; invariant for mammals; and decreasing for reptiles and amphibians. These shifts in magnitude proved robust when we accounted for an increase in the occurrence of MMEs since 1940. However, it remains unclear whether the increase in the occurrence of MMEs represents a true pattern or simply a perceived increase. Regardless, the increase in MMEs appears to be associated with a rise in disease emergence, biotoxicity, and events produced by multiple interacting stressors, yet temporal trends in MME causes varied among taxa and may be associated with increased detectability. In addition, MMEs with the largest magnitudes were those that resulted from multiple stressors, starvation, and disease. These results advance our understanding of rare demographic processes and their relationship to global and regional perturbations to natural systems.

The temporal structure of the environment may influence range expansions during climate warming.

Understanding the processes that influence range expansions during climate warming is paramount for predicting population extirpations and preparing for the arrival of non-native species. While climate warming occurs over a background of variation due to cyclical processes and irregular events, the temporal structure of the thermal environment is largely ignored when forecasting the dynamics of non-native species. Ecological theory predicts that high levels of temporal autocorrelation in the environment - relatedness between conditions occurring in close temporal proximity - will favor populations that would otherwise have an average negative growth rate by increasing the duration of favorable environmental periods. Here, we invoke such theory to explain the success of biological invasions and evaluate the hypothesis that sustained periods of high environmental temperature can act synergistically with increases in mean temperature to favor the establishment of non-native species. We conduct a 60-day field mesocosm experiment to measure the population dynamics of the non-native cladoceran zooplankter Daphnia lumholtzi and a native congener Daphnia pulex in ambient temperature environments (control), warmed with recurrent periods of high environmental temperatures (uncorrelated-warmed), or warmed with sustained periods of high environmental temperatures (autocorrelated-warmed), such that both warmed treatments exhibited the same mean temperature but exhibited different temporal structures of their thermal environments. Maximum D. lumholtzi densities in the warmed-autocorrelated treatment were threefold and eightfold higher relative to warmed-uncorrelated and control treatments, respectively. Yet, D. lumholtzi performed poorly across all experimental treatment(s) relative to D. pulex and were undetectable (by) the end of the experiment. Using mathematical models, we show that this increase in performance can occur alongside increasing temporal autocorrelation and should occur over a broad range of warming scenarios. These results provide both empirical and theoretical evidence that the temporal structure of the environment can influence the performance of species undergoing range expansions due to climate warming.

Thermal variability alters the impact of climate warming on consumer-resource systems.

Thermal variation through space and time are prominent features of ecosystems that influence processes at multiple levels of biological organization. Yet, it remains unclear how populations embedded within biological communities will respond to climate warming in thermally variable environments, particularly as climate change alters existing patterns of thermal spatial and temporal variability. As environmental temperatures increase above historical ranges, organisms may increasingly rely on extreme habitats to effectively thermoregulate. Such locations desirable in their thermal attributes (e.g., thermal refugia) are often suboptimal for resource acquisition (e.g., underground tunnels). Thus, via the expected increase in both mean temperatures and diel thermal variation, climate warming may heighten the trade-off for consumers between behaviors maximizing thermal performance and those maximizing resource acquisition. Here, we integrate behavioral, physiological, and trophic ecology to provide a general framework for understanding how temporal thermal variation, mediated by access to a thermal refugium, alters the response of consumer-resource systems to warming. We use this framework to predict how temporal variation and access to thermal refugia affect the persistence of consumers and resources during climate warming, how the quality of thermal refugia impact consumer-resource systems, and how consumer-resource systems with fast vs. slow ecological dynamics respond to warming. Our results show that the spatial thermal variability provided by refugia can elevate consumer biomass at warmer temperatures despite reducing the fraction of time consumers spend foraging, that temporal variability detrimentally impacts consumers at high environmental temperatures, and that consumer-resource systems with fast ecological dynamics are most vulnerable to climate warming. Thus, incorporating both estimates of thermal variability and species interactions may be necessary to accurately predict how populations respond to warming.

Autumn leaf subsidies influence spring dynamics of freshwater plankton communities.

While ecologists primarily focus on the immediate impact of ecological subsidies, understanding the importance of ecological subsidies requires quantifying the long-term temporal dynamics of subsidies on recipient ecosystems. Deciduous leaf litter transferred from terrestrial to aquatic ecosystems exerts both immediate and lasting effects on stream food webs. Recently, deciduous leaf additions have also been shown to be important subsidies for planktonic food webs in ponds during autumn; however, the inter-seasonal effects of autumn leaf subsidies on planktonic food webs have not been studied. We hypothesized that autumn leaf drop will affect the spring dynamics of freshwater pond food webs by altering the availability of resources, water transparency, and the metabolic state of ponds. We created leaf-added and no-leaf-added field mesocosms in autumn 2012, allowed mesocosms to ice-over for the winter, and began sampling the physical, chemical, and biological properties of mesocosms immediately following ice-off in spring 2013. At ice-off, leaf additions reduced dissolved oxygen, elevated total phosphorus concentrations and dissolved materials, and did not alter temperature or total nitrogen. These initial abiotic effects contributed to higher bacterial densities and lower chlorophyll concentrations, but by the end of spring, the abiotic environment, chlorophyll and bacterial densities converged. By contrast, zooplankton densities diverged between treatments during the spring, with leaf additions stimulating copepods but inhibiting cladocerans. We hypothesized that these differences between zooplankton orders resulted from resource shifts following leaf additions. These results suggest that leaf subsidies can alter both the short- and long-term dynamics of planktonic food webs, and highlight the importance of fully understanding how ecological subsidies are integrated into recipient food webs.

Temperature-mediated biotic interactions influence enemy release of nonnative species in warming environments.

"Enemy release" occurs when invading species suffer from interactions with pathogens, parasites, herbivores, or predators to a lesser degree than native species due to a lack of shared evolutionary history. Here we provide strong support for the hypothesis that variable thermal sensitivities between a consumer and its resources can generate temperature-dependent enemy release using both a mathematical model and a field experiment. We identify three common scenarios where changes in temperature should alter enemy release based on asymmetric responses among enemies and their resources to changes in temperature: (1) the vital rates of a shared enemy are more sensitive to changes in temperature than its resources, (2) the enemy's thermal maximum for consumption is higher than the resources' maxima for growth, and (3) the invading resource has a higher thermal maximum for growth than its native competitor. Mathematical representations indicated that warming is capable of altering enemy release in each of these three scenarios. We also tested our hypothesis using a mesocosm warming experiment in a system that exhibits variable thermal sensitivities between a predator and its native and nonnative prey. We conducted a six-week experiment manipulating the presence of Lepomis sunfish (present, absent) and water temperature (ambient, heated) using the nonnative crustacean zooplankter, Daphnia lumholtzi, whose morphological defenses reduce predation from juvenile sunfish relative to native Daphnia pulex. Our results indicate that D. lumholtzi benefited to a greater extent from the presence of Lepomis predators as temperatures increase. Taken together, our model and experiment indicate that changes in environmental temperature may directly influence the success of nonnative species and may assist with forecasting the community consequences of biological invasions in a warming world.

Interactive effects of temperature and bisphenol A on phytoplankton growth and community structure.

Environmental contamination of bisphenol A (BPA) is a widespread and multifaceted issue with vast ecological, social and economic consequences. Thus, understanding how local environmental conditions, such as temperature, interact with BPA to affect populations and community dynamics remain important areas of research. Here, we conduct laboratory experiments aimed at understanding how environmental gradients of both temperature and BPA concentration influence freshwater phytoplankton population growth and community structure. We exposed phytoplankton assemblages comprised of three common species of green algae (Chlorella vulgaris, Ankistrodesmus braunii and Scenedesmus quadricauda) as well as isolates of each individual species to three BPA concentrations (0, 2, 13 mg/L BPA) and three temperatures (18, 23, 27°C) monitoring population growth and community structure (via biovolume). We observed antagonistic interactions between BPA and warmer temperatures, such that when warmer temperatures decreased growth (observed with A. braunii), high concentrations of BPA elevated growth at these warm temperatures; however, when warmer temperatures increased growth (C. vulgaris, S. quadricauda), high BPA concentrations diminished these gains. Although BPA exposure inhibited the growth of most C. vulgaris populations, growth was not reduced in A. braunii or S. quadricauda populations exposed to 2 mg/L BPA. Phytoplankton assemblage evenness (Pielou evenness index) decreased as BPA concentration increased and was consistently lowest under 27°C. Community composition was similar in assemblages cultured under 0 and 2 mg/L BPA under 18 and 23°C but was most similar between assemblages cultured under 2 and 13 mg/L BPA under 27°C. These results indicate that local environmental temperatures can mediate the consequences of BPA for freshwater phytoplankton growth rates and community structure and that BPA can diminish potential gains of increased growth rate for warm-adapted phytoplankton species at high environmental temperatures.

Thermal sensitivity predicts the establishment success of nonnative species in a mesocosm warming experiment.

While climate change is likely to modify biological interactions between species, it is not clear how altered biotic interactions will influence specific processes such as community assembly. We show that small increases in water temperature can alter the establishment success of the nonnative, tropical zooplankton species, Daphnia lumholtzi, and suggest a general framework for understanding species establishment in the context of climate change. We compared the establishment success of D. lumholtzi and the native congener D. pulex in a mesocosm experiment manipulating temperature, food conditions, and the identity of the resident vs. establishing species. To understand if our mesocosm results could have been predicted by thermal physiology, we characterized the thermal sensitivity of each species' population growth rate and estimated the temperatures at which each species would outperform the other. As predicted by the thermal sensitivities, invading D. lumholtzi were able to establish regardless of temperature and food resources, and established more rapidly in heated mesocosms. Invading D. pulex reached higher initial abundances in ambient-temperature mesocosms but failed to establish in any heated mesocosms. These findings suggest that thermal sensitivity may predict how altered interactions between species can influence community assembly, and that higher lake temperatures will likely aid the future establishment of nonnative D. lumholtzi in North America.

The long and the short of it: Mechanisms of synchronous and compensatory dynamics across temporal scales.

Synchronous dynamics (fluctuations that occur in unison) are universal phenomena with widespread implications for ecological stability. Synchronous dynamics can amplify the destabilizing effect of environmental variability on ecosystem functions such as productivity, whereas the inverse, compensatory dynamics, can stabilize function. Here we combine simulation and empirical analyses to elucidate mechanisms that underlie patterns of synchronous versus compensatory dynamics. In both simulated and empirical communities, we show that synchronous and compensatory dynamics are not mutually exclusive but instead can vary by timescale. Our simulations identify multiple mechanisms that can generate timescale-specific patterns, including different environmental drivers, diverse life histories, dispersal, and non-stationary dynamics. We find that traditional metrics for quantifying synchronous dynamics are often biased toward long-term drivers and may miss the importance of short-term drivers. Our findings indicate key mechanisms to consider when assessing synchronous versus compensatory dynamics and our approach provides a pathway for disentangling these dynamics in natural systems.

The spatial synchrony of species richness and its relationship to ecosystem stability.

Synchrony is broadly important to population and community dynamics due to its ubiquity and implications for extinction dynamics, system stability, and species diversity. Investigations of synchrony in community ecology have tended to focus on covariance in the abundances of multiple species in a single location. Yet, the importance of regional environmental variation and spatial processes in community dynamics suggests that community properties, such as species richness, could fluctuate synchronously across patches in a metacommunity, in an analog of population spatial synchrony. Here, we test the prevalence of this phenomenon and the conditions under which it may occur using theoretical simulations and empirical data from 20 marine and terrestrial metacommunities. Additionally, given the importance of biodiversity for stability of ecosystem function, we posit that spatial synchrony in species richness is strongly related to stability. Our findings show that metacommunities often exhibit spatial synchrony in species richness. We also found that richness synchrony can be driven by environmental stochasticity and dispersal, two mechanisms of population spatial synchrony. Richness synchrony also depended on community structure, including species evenness and beta diversity. Strikingly, ecosystem stability was more strongly related to richness synchrony than to species richness itself, likely because richness synchrony integrates information about community processes and environmental forcing. Our study highlights a new approach for studying spatiotemporal community dynamics and emphasizes the spatial dimensions of community dynamics and stability.

Course-based undergraduate research experiences in a remote setting: Two case studies documenting implementation and student perceptions.

Inquiry-based components of ecology curricula can be valuable, exposing students to what it means to do science, from conceiving of a meaningful question to effectively disseminating results to an audience. Here, we describe two approaches for implementing independent, remote research for undergraduates enacted in the spring semester of 2020 at Reed College in Portland, OR, reporting case studies from an intermediate-level ecology course and an interdisciplinary environmental science course. We report on both the challenges as well as the novel opportunities for independent research projects in such a setting, the details of how projects were implemented, the tools and resources that may help facilitate such endeavors, as well as perceptions on the effectiveness of this endeavor by students. As institutes of higher education continue to operate in an online learning environment, we hope these materials help spark a discussion about how to engage in meaningful research experiences as part of coursework in the COVID-19 era and beyond.

Life in the Frequency Domain: the Biological Impacts of Changes in Climate Variability at Multiple Time Scales.

Over the last few decades, biologists have made substantial progress in understanding relationships between changing climates and organism performance. Much of this work has focused on temperature because it is the best kept of climatic records, in many locations it is predicted to keep rising into the future, and it has profound effects on the physiology, performance, and ecology of organisms, especially ectothermic organisms which make up the vast majority of life on Earth. Nevertheless, much of the existing literature on temperature-organism interactions relies on mean temperatures. In reality, most organisms do not directly experience mean temperatures; rather, they experience variation in temperature over many time scales, from seconds to years. We propose to shift the focus more directly on patterns of temperature variation, rather than on means per se, and present a framework both for analyzing temporal patterns of temperature variation and for incorporating those patterns into predictions about organismal biology. In particular, we advocate using the Fourier transform to decompose temperature time series into their component sinusoids, thus allowing transformations between the time and frequency domains. This approach provides (1) standardized ways of visualizing the contributions that different frequencies make to total temporal variation; (2) the ability to assess how patterns of temperature variation have changed over the past half century and may change into the future; and (3) clear approaches to manipulating temporal time series to ask "what if" questions about the potential effects of future climates. We first summarize global patterns of change in temperature variation over the past 40 years; we find meaningful changes in variation at the half day to yearly times scales. We then demonstrate the utility of the Fourier framework by exploring how power added to different frequencies alters the overall incidence of long-term waves of high and low temperatures, and find that power added to the lowest frequencies greatly increases the probability of long-term heat and cold waves. Finally, we review what is known about the time scales over which organismal thermal performance curves change in response to variation in the thermal environment. We conclude that integrating information characterizing both the frequency spectra of temperature time series and the time scales of resulting physiological change offers a powerful new avenue for relating climate, and climate change, to the future performance of ectothermic organisms.

Type I interferons induce autophagy in certain human cancer cell lines.

Autophagy is an evolutionarily conserved cellular recycling mechanism that occurs at a basal level in all cells. It can be further induced by various stimuli including starvation, hypoxia, and treatment with cytokines such as IFNG/IFNγ and TGFB/TGFß. Type I IFNs are proteins that induce an antiviral state in cells. They also have antiproliferative, proapoptotic and immunomodulatory activities. We investigated whether type I IFN can also induce autophagy in multiple human cell lines. We found that treatment with IFNA2c/IFNα2c and IFNB/IFNß induces autophagy by 24 h in Daudi B cells, as indicated by an increase of autophagy markers MAP1LC3-II, ATG12-ATG5 complexes, and a decrease of SQSTM1 expression. An increase of MAP1LC3-II was also detected 48 h post-IFNA2c treatment in HeLa S3, MDA-MB-231, T98G and A549 cell lines. The presence of autophagosomes in selected cell lines exposed to type I IFN was confirmed by electron microscopy analysis. Increased expression of autophagy markers correlated with inhibition of MTORC1 in Daudi cells, as well as inhibition of cancer cell proliferation and changes in cell cycle progression. Concomitant blockade of either MTOR or PI3K-AKT signaling in Daudi and T98G cells treated with IFNA2c increased the level of MAP1LC3-II, indicating that the PI3K-AKT-MTORC1 signaling pathway may modulate IFN-induced autophagy in these cells. Taken together, our findings demonstrated a novel function of type I IFN as an inducer of autophagy in multiple cell lines.