The Asymmetric Response Concept explains ecological consequences of multiple stressor exposure and release.

Our capacity to predict trajectories of ecosystem degradation and recovery is limited, especially when impairments are caused by multiple stressors. Recovery may be fast or slow and either complete or partial, sometimes result in novel ecosystem states or even fail completely. Here, we introduce the Asymmetric Response Concept (ARC) that provides a basis for exploring and predicting the pace and magnitude of ecological responses to, and release from, multiple stressors. The ARC holds that three key mechanisms govern population, community and ecosystem trajectories. Stress tolerance is the main mechanism determining responses to increasing stressor intensity, whereas dispersal and biotic interactions predominantly govern responses to the release from stressors. The shifting importance of these mechanisms creates asymmetries between the ecological trajectories that follow increasing and decreasing stressor intensities. This recognition helps to understand multiple stressor impacts and to predict which measures will restore communities that are resistant to restoration.

Interaction-Specific Changes in the Transcriptome of Polynucleobacter asymbioticus Caused by Varying Protistan Communities.

We studied the impact of protist grazing and exudation on the growth and transcriptomic response of the prokaryotic prey species Polynucleobacter asymbioticus. Different single- and multi-species communities of chrysophytes were used to determine a species-specific response to the predators and the effect of chrysophyte diversity. We sequenced the mRNA of Pn. asymbioticus in communities with three single chrysophyte species (Chlorochromonas danica, Poterioochromonas malhamensis and Poteriospumella lacustris) and all combinations. The molecular responses of Pn. asymbioticus significantly changed in the presence of predators with different trophic modes and combinations of species. In the single-species samples we observed significant differences related to the relative importance of grazing and exudation in the protist-bacteria interaction, i.e., to the presence of either the heterotrophic Ps. lacustris or the mixotrophic C. danica. When grazing dominates the interaction, as in the presence of Ps. lacustris, genes acting in stress response are up-regulated. Further genes associated with transcription and translation are down-regulated indicating a reduced growth of Pn. asymbioticus. In contrast, when the potential use of algal exudates dominates the interaction, genes affiliated with iron transport are up-regulated. Rapid phototrophic growth of chrysophytes, with a high demand on soluble iron, could thus lead to iron-limitation and cause changes in the iron metabolism of Pn. asymbioticus. Additionally, we observe a benefit for Pn. asymbioticus from a more diverse protistan community, which could be due to shifts in the relative importance of phototrophy in the mixotrophic chrysophytes when competing for food with other species. Our study highlights the importance of biotic interactions and the specificity of such interactions, in particular the differential effect of grazing and algal exudation in the interaction of bacteria with mixotrophic protists.

Delayed Chemical Defense: Timely Expulsion of Herbivores Can Reduce Competition with Neighboring Plants.

Time delays in plant responses to insect herbivory are thought to be the principal disadvantage of induced over constitutive defenses, suggesting that there should be strong selection for rapid responses. However, observed time delays between the onset of herbivory and defense induction vary considerably among plants. We postulate that strong competition with conspecifics is an important codeterminant of the cost-benefit balance for induced responses. There may be a benefit to the plant to delay mounting a full defense response until the herbivore larvae are mobile enough to leave and large enough to cause severe damage to neighboring plants. Thus, delayed responses could reduce the competitive pressure on the focal plant. To explore this idea, we developed an individual-based model using data from wild tobacco, Nicotiana attenuata, and its specialized herbivore, Manduca sexta. Chemical defense was assumed to be costly in terms of reduced plant growth. We used a genetic algorithm with the plant's delay time as a heritable trait. A stationary distribution of delay times emerged, which under high herbivore densities peaked at higher values, which were related to the time larvae need to grow large enough to severely damage neighboring plants. Plants may thus tip the competitive balance by expelling insect herbivores to move to adjacent plants when the herbivores are most damaging. Thus, herbivores become part of a plant's strategy for reducing competition and increasing fitness.

Silver stress differentially affects growth of phototrophic and heterotrophic chrysomonad flagellate populations.

Silver ions are among the predominant anthropogenic introduced pollutants in aquatic systems. As silver has effects on species at all trophic levels the community composition in aquatic habitats can be changed as a result of silver stress. The response of planktonic protists to environmental stressors is particularly important as they act both as producers and consumers in complex planktonic communities. Chrysomonad flagellates are of major interest, since this group includes heterotrophic, mixotrophic and phototrophic taxa, and therefore allows analysis of silver stress in organisms with contrasting nutritional strategies independent of a potential taxonomic bias. In a series of lab experiments, we compared the response of different trophic chrysophyte strains to low (5 µg L-1), medium (10 µg L-1) and high (20 µg L-1) nominal Ag concentrations in combination with changes in temperature and light intensity (phototrophs), temperature and food concentration (heterotrophs), or a combination of the above settings (mixotrophs). All tested strains were negatively affected by silver in their growth rates. The phototrophic strains reacted strongly to silver stress, whereas light intensity and temperature had only minor effects on growth rates. For heterotrophic strains, high food concentration toned down the effect of silver, whereas temperatures outside the growth optimum had a combined stress effect. The mixotrophic strains reacted differently depending on whether their nutritional mode was dominated by heterotrophy or by phototrophy. The precise response pattern across all variables was uniquely different for every single species we tested. The present work contributes to a deeper understanding of the effects of environmental stressors on complex planktonic communities. It indicates that silver will negatively impact planktonic communities and may create shifts in their composition and functioning.

Novel Indicators for the Quantification of Resilience in Critical Material Supply Chains, with a 2010 Rare Earth Crisis Case Study.

We introduce several new resilience metrics for quantifying the resilience of critical material supply chains to disruptions and validate these metrics using the 2010 rare earth element (REE) crisis as a case study. Our method is a novel application of Event Sequence Analysis, supplemented with interviews of actors across the entire supply chain. We discuss resilience mechanisms in quantitative terms-time lags, response speeds, and maximum magnitudes-and in light of cultural differences between Japanese and European corporate practice. This quantification is crucial if resilience is ever to be taken into account in criticality assessments and a step toward determining supply and demand elasticities in the REE supply chain. We find that the REE system showed resilience mainly through substitution and increased non-Chinese primary production, with a distinct role for stockpiling. Overall, annual substitution rates reached 10% of total demand. Non-Chinese primary production ramped up at a speed of 4% of total market volume per year. The compound effect of these mechanisms was that recovery from the 2010 disruption took two years. The supply disruption did not nudge a system toward an appreciable degree of recycling. This finding has important implications for the circular economy concept, indicating that quite a long period of sustained material constraints will be necessary for a production-consumption system to naturally evolve toward a circular configuration.

Comprehensive transcriptome analysis provides new insights into nutritional strategies and phylogenetic relationships of chrysophytes.

BACKGROUND: Chrysophytes are protist model species in ecology and ecophysiology and important grazers of bacteria-sized microorganisms and primary producers. However, they have not yet been investigated in detail at the molecular level, and no genomic and only little transcriptomic information is available. Chrysophytes exhibit different trophic modes: while phototrophic chrysophytes perform only photosynthesis, mixotrophs can gain carbon from bacterial food as well as from photosynthesis, and heterotrophs solely feed on bacteria-sized microorganisms. Recent phylogenies and megasystematics demonstrate an immense complexity of eukaryotic diversity with numerous transitions between phototrophic and heterotrophic organisms. The question we aim to answer is how the diverse nutritional strategies, accompanied or brought about by a reduction of the plasmid and size reduction in heterotrophic strains, affect physiology and molecular processes. RESULTS: We sequenced the mRNA of 18 chrysophyte strains on the Illumina HiSeq platform and analysed the transcriptomes to determine relations between the trophic mode (mixotrophic vs. heterotrophic) and gene expression. We observed an enrichment of genes for photosynthesis, porphyrin and chlorophyll metabolism for phototrophic and mixotrophic strains that can perform photosynthesis. Genes involved in nutrient absorption, environmental information processing and various transporters (e.g., monosaccharide, peptide, lipid transporters) were present or highly expressed only in heterotrophic strains that have to sense, digest and absorb bacterial food. We furthermore present a transcriptome-based alignment-free phylogeny construction approach using transcripts assembled from short reads to determine the evolutionary relationships between the strains and the possible influence of nutritional strategies on the reconstructed phylogeny. We discuss the resulting phylogenies in comparison to those from established approaches based on ribosomal RNA and orthologous genes. Finally, we make functionally annotated reference transcriptomes of each strain available to the community, significantly enhancing publicly available data on Chrysophyceae. CONCLUSIONS: Our study is the first comprehensive transcriptomic characterisation of a diverse set of Chrysophyceaen strains. In addition, we showcase the possibility of inferring phylogenies from assembled transcriptomes using an alignment-free approach. The raw and functionally annotated data we provide will prove beneficial for further examination of the diversity within this taxon. Our molecular characterisation of different trophic modes presents a first such example.

Extreme heat changes post-heat wave community reassembly.

Climate forecasts project further increases in extremely high-temperature events. These present threats to biodiversity, as they promote population declines and local species extinctions. This implies that ecological communities will need to rely more strongly on recovery processes, such as recolonization from a meta-community context. It is poorly understood how differences in extreme event intensity change the outcome of subsequent community reassembly and if such extremes modify the biotic environment in ways that would prevent the successful re-establishment of lost species. We studied replicated aquatic communities consisting of algae and herbivorous rotifers in a design that involved a control and two different heat wave intensity treatments (29°C and 39°C). Animal species that suffered heat-induced extinction were subsequently re-introduced at the same time and density, in each of the two treatments. The 39°C treatment led to community closure in all replicates, meaning that a previously successful herbivore species could not re-establish itself in the postheat wave community. In contrast, such closure never occurred after a 29°C event. Heat wave intensity determined the number of herbivore extinctions and strongly affected algal relative abundances. Re-introduced herbivore species were thus confronted with significantly different food environments. This ecological legacy generated by heat wave intensity led to differences in the failure or success of herbivore species re-introductions. Reassembly was significantly more variable, and hence less predictable, after an extreme heat wave, and was more canalized after a moderate one. Our results pertain to relatively simple communities, but they suggest that ecological legacies introduced by extremely high-temperature events may change subsequent ecological recovery and even prevent the successful re-establishment of lost species. Knowing the processes promoting and preventing ecological recovery is crucial to the success of species re-introduction programs and to our ability to restore ecosystems damaged by environmental extremes.

Framework for resilience in material supply chains, with a case study from the 2010 Rare Earth Crisis.

In 2010, Chinese export restrictions caused the price of the rare earth element neodymium to increase by a factor of 10, only to return to almost normal levels in the following months. This despite the fact that the restrictions were not lifted. The significant price peak shows that this material supply chain was only weakly resistant to a major supply disruption. However, the fact that prices rapidly returned to lower levels implies a certain resilience. With the help of a novel approach, based on resilience theory combined with a material flow analysis (MFA) based representation of the neodymium magnet (NdFeB) supply chain, we show that supply chain resilience is composed of various mechanisms, including (a) resistance, (b) rapidity, and (c) flexibility, that originate from different parts of the supply chain. We make recommendations to improve the capacity of the NdFeB system to deal with future disruptions and discuss potential generalities for the resilience of other material supply chains.

Food web persistence is enhanced by non-trophic interactions.

The strength of interspecific interactions is often proposed to affect food web stability, with weaker interactions increasing the persistence of species, and food webs as a whole. However, the mechanisms that modify interaction strengths, and their effects on food web persistence are not fully understood. Using food webs containing different combinations of predator, prey, and nonprey species, we investigated how predation risk of susceptible prey is affected by the presence of species not directly trophically linked to either predators or prey. We predicted that indirect alterations to the strength of trophic interactions translate to changes in persistence time of extinction-prone species. We assembled interaction webs of protist consumers and turbellarian predators with eight different combinations of prey, predators and nonprey species, and recorded abundances for over 130 prey generations. Persistence of predation-susceptible species was increased by the presence of nonprey. Furthermore, multiple nonprey species acted synergistically to increase prey persistence, such that persistence was greater than would be predicted from the dynamics of simpler food webs. We also found evidence suggesting increased food web complexity may weaken interspecific competition, increasing persistence of poorer competitors. Our results demonstrate that persistence times in complex food webs cannot be predicted from the dynamics of simplified systems, and that species not directly involved in consumptive interactions likely play key roles in maintaining persistence. Global species diversity is currently declining at an unprecedented rate and our findings reveal that concurrent loss of species that modify trophic interactions may have unpredictable consequences for food web stability.

Warming-induced changes in predation, extinction and invasion in an ectotherm food web.

Climate change will alter the forces of predation and competition in temperate ectotherm food webs. This may increase local extinction rates, change the fate of invasions and impede species reintroductions into communities. Invasion success could be modulated by traits (e.g., defenses) and adaptations to climate. We studied how different temperatures affect the time until extinction of species, using bitrophic and tritrophic planktonic food webs to evaluate the relative importance of predatory overexploitation and competitive exclusion, at 15 and 25 °C. In addition, we tested how inclusion of a subtropical as opposed to a temperate strain in this model food web affects times until extinction. Further, we studied the invasion success of the temperate rotifer Brachionus calyciflorus into the planktonic food web at 15 and 25 °C on five consecutive introduction dates, during which the relative forces of predation and competition differed. A higher temperature dramatically shortened times until extinction of all herbivore species due to carnivorous overexploitation in tritrophic systems. Surprisingly, warming did not increase rates of competitive exclusion among the tested herbivore species in bitrophic communities. Including a subtropical herbivore strain reduced top-down control by the carnivore at high temperature. Invasion attempts of temperate B. calyciflorus into the food web always succeeded at 15 °C, but consistently failed at 25 °C due to voracious overexploitation by the carnivore. Pre-induction of defenses (spines) in B. calyciflorus before the invasion attempt did not change its invasion success at the high temperature. We conclude that high temperatures may promote local extinctions in temperate ectotherms and reduce their chances of successful recovery.

When to defend: antipredator defenses and the predation sequence.

Some authors have suggested that prey species stand to benefit most by defending as early as possible during predator-prey encounters, but species in nature employ antipredator defenses at various stages of interactions with their predators. Whether it is generally most advantageous to defend early or late during such encounters is an open theoretical question. We model conditions under which a prey species might evolve early or late defenses in response to predation. Adapting a two-prey, one-predator Rosenzweig-MacArthur system of differential equations, we analyze the effects of modified antipredator defenses (and their associated costs) on the ability of a new prey type to invade the one-prey, one-predator limiting system at equilibrium. We show that the outcome, in terms of invasion potential, is crucially dependent on the ratio of the prey's proportional population growth rate to the cost of predator encounters.

Heated relations: temperature-mediated shifts in consumption across trophic levels.

A rise in temperature will intensify the feeding links involving ectotherms in food webs. However, it is unclear how the effects will quantitatively differ between the plant-herbivore and herbivore-carnivore interface. To test how warming could differentially affect rates of herbivory and carnivory, we studied trophic interaction strength in a food chain comprised of green algae, herbivorous rotifers and carnivorous rotifers at 10, 15, 20 and 25°C. We found significant warming-induced changes in feeding by both herbivorous and carnivorous rotifers, but these responses occurred at different parts of the entire temperature gradient. The strongest response of the per capita herbivore's ingestion rate occurred due to an increase in temperature from 15 to 20°C (1.9 fold: from 834 to 1611 algal cells per h(-1)) and of the per capita carnivore's ingestion rate from 20 to 25°C (1.6 fold: from 1.5 to 2.5 prey h(-1)). Handling time, an important component of a consumer's functional response, significantly decreased from 15 to 20°C in herbivorous rotifers. In contrast, it decreased from 20 to 25°C in carnivorous rotifers. Attack rates significantly and strongly increased from 10 to 25°C in the herbivorous animals, but not at all in the carnivores. Our results exemplify how the relative forces of top-down control exerted by herbivores and carnivores may strongly shift under global warming. But warming, and its magnitude, are not the only issue: If our results would prove to be representative, shifts in ectotherm interactions will quantitatively differ when a 5°C increase starts out from a low, intermediate or high initial temperature. This would imply that warming could have different effects on the relative forces of carnivory and herbivory in habitats differing in average temperature, as would exist at different altitudes and latitudes.

Diversity, functional similarity, and top-down control drive synchronization and the reliability of ecosystem function.

The concept that diversity promotes reliability of ecosystem function depends on the pattern that community-level biomass shows lower temporal variability than species-level biomasses. However, this pattern is not universal, as it relies on compensatory or independent species dynamics. When in contrast within-trophic level synchronization occurs, variability of community biomass will approach population-level variability. Current knowledge fails to integrate how species richness, functional distance between species, and the relative importance of predation and competition combine to drive synchronization at different trophic levels. Here we clarify these mechanisms. Intense competition promotes compensatory dynamics in prey, but predators may at the same time increasingly synchronize, under increasing species richness and functional similarity. In contrast, predators and prey both show perfect synchronization under strong top-down control, which is promoted by a combination of low functional distance and high net growth potential of predators. Under such conditions, community-level biomass variability peaks, with major negative consequences for reliability of ecosystem function.

Testing the paradox of enrichment along a land use gradient in a multitrophic aboveground and belowground community.

In the light of ongoing land use changes, it is important to understand how multitrophic communities perform at different land use intensities. The paradox of enrichment predicts that fertilization leads to destabilization and extinction of predator-prey systems. We tested this prediction for a land use intensity gradient from natural to highly fertilized agricultural ecosystems. We included multiple aboveground and belowground trophic levels and land use-dependent searching efficiencies of insects. To overcome logistic constraints of field experiments, we used a successfully validated simulation model to investigate plant responses to removal of herbivores and their enemies. Consistent with our predictions, instability measured by herbivore-induced plant mortality increased with increasing land use intensity. Simultaneously, the balance between herbivores and natural enemies turned increasingly towards herbivore dominance and natural enemy failure. Under natural conditions, there were more frequently significant effects of belowground herbivores and their natural enemies on plant performance, whereas there were more aboveground effects in agroecosystems. This result was partly due to the "boom-bust" behavior of the shoot herbivore population. Plant responses to herbivore or natural enemy removal were much more abrupt than the imposed smooth land use intensity gradient. This may be due to the presence of multiple trophic levels aboveground and belowground. Our model suggests that destabilization and extinction are more likely to occur in agroecosystems than in natural communities, but the shape of the relationship is nonlinear under the influence of multiple trophic interactions.

The good, the bad and the plenty: interactive effects of food quality and quantity on the growth of different Daphnia species.

Effects of food quality and quantity on consumers are neither independent nor interchangeable. Although consumer growth and reproduction show strong variation in relation to both food quality and quantity, the effects of food quality or food quantity have usually been studied in isolation. In two experiments, we studied the growth and reproduction in three filter-feeding freshwater zooplankton species, i.e. Daphnia galeata x hyalina, D. pulicaria and D. magna, on their algal food (Scenedesmus obliquus), varying in carbon to phosphorus (C∶P) ratios and quantities (concentrations). In the first experiment, we found a strong positive effect of the phosphorus content of food on growth of Daphnia, both in their early and late juvenile development. Variation in the relationship between the P-content of animals and their growth rate reflected interspecific differences in nutrient requirements. Although growth rates typically decreased as development neared maturation, this did not affect these species-specific couplings between growth rate and Daphnia P-content. In the second experiment, we examined the effects of food quality on Daphnia growth at different levels of food quantity. With the same decrease in P-content of food, species with higher estimated P-content at zero growth showed a larger increase in threshold food concentrations (i.e. food concentration sufficient to meet metabolic requirements but not growth). These results suggest that physiological processes such as maintenance and growth may in combination explain effects of food quality and quantity on consumers. Our study shows that differences in response to variation in food quality and quantity exist between species. As a consequence, species-specific effects of food quality on consumer growth will also determine how species deal with varying food levels, which has implications for resource-consumer interactions.

Functional responses modified by predator density.

Realistic functional responses are required for accurate model predictions at the community level. However, controversy remains regarding which types of dependencies need to be included in functional response models. Several studies have shown an effect of very high predator densities on per capita predation rates, but it is unclear whether this predator dependence is also important at low predator densities. We fit integrated functional response models to predation data from 4-h experiments where we had varied both predator and prey densities. Using an information theoretic approach we show that the best-fit model includes moderate predator dependence, which was equally strong even at low predator densities. The best fits of Beddington-DeAngelis and Arditi-Akçakaya functional responses were closely followed by the fit of the Arditi-Ginzburg model. A Holling type III functional response did not describe the data well. In addition, independent behavioral observations revealed high encounter rates between predators. We quantified the number of encounters between predators and the time the focal predator spent interacting with other individuals per encounter. This time "wasted" on conspecifics reduced the total time available for foraging and may therefore account for lower predation rates at higher predator densities. Our findings imply that ecological theory needs to take realistic levels of predator dependence into account.

Inducible defenses, competition and shared predation in planktonic food chains.

Ecologists have long debated the role of predation in mediating the coexistence of prey species. Theory has mainly taken a bitrophic perspective that excludes the effects of inducible defenses at different trophic levels. However, inducible defenses could either limit or enhance the effects of predation on coexistence, by means of effects on bottom-up control and population stability. Our aim was to investigate how inducible defenses at different trophic levels affect the possibilities for predator-mediated coexistence, as opposed to competitive exclusion, in replicated experimental plankton communities. In particular, we analyzed how the presence or absence of inducible defenses in algal basal prey affected the outcome of competition between an inducible defended and an undefended herbivore, in the presence or absence of a carnivore. We found the undefended herbivore to be a superior competitor in the absence of predation. This outcome was reversed in the presence of a shared carnivore: populations of the undefended herbivore then strongly declined. The extent of this population decline differed between food webs based on undefended as opposed to inducible defended algal prey. In the former the undefended herbivore became undetectable for most of the duration of the experiment. In the latter the undefended herbivore also crashed to low densities, but it could still be detected during most of the experiment. In food webs based on inducible defended algae, the carnivore failed to reach high densities and exerted weaker top-down control on the two competing herbivores. We conclude that the inducible defense in one of our two competing herbivores allowed the outcome of competition to be reversed when a shared carnivore was added. Inducible defenses in algae did not change this outcome, but they significantly delayed extinction of the undefended herbivore. Predation itself did not promote coexistence in these experimental plankton communities.

Induced defenses in herbivores and plants differentially modulate a trophic cascade.

Inducible defenses are dynamic traits that modulate the strength of both plant-herbivore and herbivore-carnivore interactions. Surprisingly few studies have considered the relative contributions of induced plant and herbivore defenses to the overall balance of bottom-up and top-down control. Here we compare trophic cascade strengths using replicated two-level and three-level plankton communities in which we systematically varied the presence or absence of induced defenses at the plant and/or herbivore levels. Our results show that a trophic cascade, i.e., significantly higher plant biomass in three-level than in two-level food chains, occurred whenever herbivores were undefended against carnivores. Trophic cascades did not occur when herbivores exhibited an induced defense. This pattern was obtained irrespective of the presence or absence of induced defenses at the plant level. We thus found that herbivore defenses, not plant defenses, had an overriding effect on cascade strength. We discuss these results in relation to variation in cascade strengths in natural communities.

Species diversity modulates predation.

Predation occurs in a context defined by both prey and non-prey species. At present it is largely unknown how species diversity in general, and species that are not included in a predator's diet in particular, modify predator-prey interactions. Therefore we studied how both the density and diversity of non-prey species modified predation rates in experimental microcosms. We found that even a low density of a single nonprey species depressed the asymptote of a predator's functional response. Increases in the density and diversity of non-prey species further reduced predation rates to very low levels. Controls showed that this diversity effect was not due to the identity of any of the non-prey species. Our results establish that both the density and diversity of species outside a predator's diet can significantly weaken the strength of predator-prey interactions. These results have major implications for ecological theory on species interactions in simple vs. complex communities. We discuss our findings in terms of the relationship between diversity and stability.