Warming impairs trophic transfer efficiency in a long-term field experiment.

In ecosystems, the efficiency of energy transfer from resources to consumers determines the biomass structure of food webs. As a general rule, about 10% of the energy produced in one trophic level makes it up to the next1-3. Recent theory suggests that this energy transfer could be further constrained if rising temperatures increase metabolic growth costs4, although experimental confirmation in whole ecosystems is lacking. Here we quantify nitrogen transfer efficiency-a proxy for overall energy transfer-in freshwater plankton in artificial ponds that have been exposed to seven years of experimental warming. We provide direct experimental evidence that, relative to ambient conditions, 4 °C of warming can decrease trophic transfer efficiency by up to 56%. In addition, the biomass of both phytoplankton and zooplankton was lower in the warmed ponds, which indicates major shifts in energy uptake, transformation and transfer5,6. These findings reconcile observed warming-driven changes in individual-level growth costs and in carbon-use efficiency across diverse taxa4,7-10 with increases in the ratio of total respiration to gross primary production at the ecosystem level11-13. Our results imply that an increasing proportion of the carbon fixed by photosynthesis will be lost to the atmosphere as the planet warms, impairing energy flux through food chains, which will have negative implications for larger consumers and for the functioning of entire ecosystems.

Extra terrestrials: drought creates niche space for rare invertebrates in a large-scale and long-term field experiment.

Freshwater habitats are drying more frequently and for longer under the combined pressures of climate change and overabstraction. Unsurprisingly, many aquatic species decline or become locally extinct as their benthic habitat is lost during stream droughts, but less is known about the potential 'winners': those terrestrial species that may exploit emerging niches in drying riverbeds. In particular, we do not know how these transient ecotones will respond as droughts become more extreme in the future. To find out we used a large-scale, long-term mesocosm experiment spanning a wide gradient of drought intensity, from permanent flows to full streambed dewatering, and analysed terrestrial invertebrate community assembly after 1 year. Droughts that caused stream fragmentation gave rise to the most diverse terrestrial invertebrate assemblages, including 10 species with UK conservation designations, and high species turnover between experimental channels. Droughts that caused streambed dewatering produced lower terrestrial invertebrate richness, suggesting that the persistence of instream pools may benefit these taxa as well as aquatic biota. Particularly intense droughts may therefore yield relatively few 'winners' among either aquatic or terrestrial species, indicating that the threat to riverine biodiversity from future drought intensification could be more pervasive than widely acknowledged.

Local stressors mask the effects of warming in freshwater ecosystems.

Climate warming is a ubiquitous stressor in freshwater ecosystems, yet its interactive effects with other stressors are poorly understood. We address this knowledge gap by testing the ability of three contrasting null models to predict the joint impacts of warming and a range of other aquatic stressors using a new database of 296 experimental combinations. Despite concerns that stressors will interact to cause synergisms, we found that net impacts were usually best explained by the effect of the stronger stressor alone (the dominance null model), especially if this stressor was a local disturbance associated with human land use. Prediction accuracy depended on stressor identity and how asymmetric stressors were in the magnitude of their effects. These findings suggest we can effectively predict the impacts of multiple stressors by focusing on the stronger stressor, as habitat alteration, nutrients and contamination often override the biological consequences of higher temperatures in freshwater ecosystems.

Systematic variation in food web body-size structure linked to external subsidies.

The relationship between body mass (M) and size class abundance (N) depicts patterns of community structure and energy flow through food webs. While the general assumption is that M and N scale linearly (on log-log axes), nonlinearity is regularly observed in natural systems, and is theorized to be driven by nonlinear scaling of trophic level (TL) with M resulting in the rapid transfer of energy to consumers in certain size classes. We tested this hypothesis with data from 31 stream food webs. We predicted that allochthonous subsidies higher in the web results in nonlinear M-TL relationships and systematic abundance peaks in macroinvertebrate and fish size classes (latter containing salmonids), that exploit terrestrial plant material and terrestrial invertebrates, respectively. Indeed, both M-N and M-TL significantly deviated from linear relationships and the observed curvature in M-TL scaling was inversely related to that observed in M-N relationships. Systemic peaks in M-N, and troughs in M-TL occurred in size classes dominated by generalist invertebrates, and brown trout. Our study reveals how allochthonous resources entering high in the web systematically shape community size structure and demonstrates the relevance of a generalized metabolic scaling model for understanding patterns of energy transfer in energetically 'open' food webs.

Extreme drought pushes stream invertebrate communities over functional thresholds.

Functional traits are increasingly being used to predict extinction risks and range shifts under long-term climate change scenarios, but have rarely been used to study vulnerability to extreme climatic events, such as supraseasonal droughts. In streams, drought intensification can cross thresholds of habitat loss, where marginal changes in environmental conditions trigger disproportionate biotic responses. However, these thresholds have been studied only from a structural perspective, and the existence of functional nonlinearity remains unknown. We explored trends in invertebrate community functional traits along a gradient of drought intensity, simulated over 18 months, using mesocosms analogous to lowland headwater streams. We modelled the responses of 16 traits based on a priori predictions of trait filtering by drought, and also examined the responses of trait profile groups (TPGs) identified via hierarchical cluster analysis. As responses to drought intensification were both linear and nonlinear, generalized additive models (GAMs) were chosen to model response curves, with the slopes of fitted splines used to detect functional thresholds during drought. Drought triggered significant responses in 12 (75%) of the a priori-selected traits. Behavioural traits describing movement (dispersal, locomotion) and diet were sensitive to moderate-intensity drought, as channels fragmented into isolated pools. By comparison, morphological and physiological traits showed little response until surface water was lost, at which point we observed sudden shifts in body size, respiration mode and thermal tolerance. Responses varied widely among TPGs, ranging from population collapses of non-aerial dispersers as channels fragmented to irruptions of small, eurythermic dietary generalists upon extreme dewatering. Our study demonstrates for the first time that relatively small changes in drought intensity can trigger disproportionately large functional shifts in stream communities, suggesting that traits-based approaches could be particularly useful for diagnosing catastrophic ecological responses to global change.

Consistent temperature dependence of functional response parameters and their use in predicting population abundance.

Global warming is one of the greatest threats to the persistence of populations: increased metabolic demands should strengthen pairwise species interactions, which could destabilize food webs at the higher organizational levels. Quantifying the temperature dependence of consumer-resource interactions is thus essential for predicting ecological responses to warming. We explored feeding interactions between different predator-prey pairs in controlled-temperature chambers and in a system of naturally heated streams. We found consistent temperature dependence of attack rates across experimental settings, though the magnitude and activation energy of attack rate were specific to each predator, which varied in mobility and foraging mode. We used these parameters along with metabolic rate measurements to estimate energetic efficiency and population abundance with warming. Energetic efficiency accurately estimated field abundance of a mobile predator that struggled to meet its metabolic demands, but was a poor predictor for a sedentary predator that operated well below its energetic limits. Temperature effects on population abundance may thus be strongly dependent on whether organisms are regulated by their own energy intake or interspecific interactions. Given the widespread use of functional response parameters in ecological modelling, reconciling outcomes from laboratory and field studies increases the confidence and precision with which we can predict warming impacts on natural systems.

Bending the rules: exploitation of allochthonous resources by a top-predator modifies size-abundance scaling in stream food webs.

Body mass-abundance (M-N) allometries provide a key measure of community structure, and deviations from scaling predictions could reveal how cross-ecosystem subsidies alter food webs. For 31 streams across the UK, we tested the hypothesis that linear log-log M-N scaling is shallower than that predicted by allometric scaling theory when top predators have access to allochthonous prey. These streams all contained a common and widespread top predator (brown trout) that regularly feeds on terrestrial prey and, as hypothesised, deviations from predicted scaling increased with its dominance of the fish assemblage. Our study identifies a key beneficiary of cross-ecosystem subsidies at the top of stream food webs and elucidates how these inputs can reshape the size-structure of these 'open' systems.

Metabarcoding of freshwater invertebrates to detect the effects of a pesticide spill.

Biomonitoring underpins the environmental assessment of freshwater ecosystems and guides management and conservation. Current methodology for surveys of (macro)invertebrates uses coarse taxonomic identification where species-level resolution is difficult to obtain. Next-generation sequencing of entire assemblages (metabarcoding) provides a new approach for species detection, but requires further validation. We used metabarcoding of invertebrate assemblages with two fragments of the cox1 "barcode" and partial nuclear ribosomal (SSU) genes, to assess the effects of a pesticide spill in the River Kennet (southern England). Operational taxonomic unit (OTU) recovery was tested under 72 parameters (read denoising, filtering, pair merging and clustering). Similar taxonomic profiles were obtained under a broad range of parameters. The SSU marker recovered Platyhelminthes and Nematoda, missed by cox1, while Rotifera were only amplified with cox1. A reference set was created from all available barcode entries for Arthropoda in the BOLD database and clustered into OTUs. The River Kennet metabarcoding produced matches to 207 of these reference OTUs, five times the number of species recognized with morphological monitoring. The increase was due to the following: greater taxonomic resolution (e.g., splitting a single morphotaxon "Chironomidae" into 55 named OTUs); splitting of Linnaean binomials into multiple molecular OTUs; and the use of a filtration-flotation protocol for extraction of minute specimens (meiofauna). Community analyses revealed strong differences between "impacted" vs. "control" samples, detectable with each gene marker, for each major taxonomic group, and for meio- and macrofaunal samples separately. Thus, highly resolved taxonomic data can be extracted at a fraction of the time and cost of traditional nonmolecular methods, opening new avenues for freshwater invertebrate biodiversity monitoring and molecular ecology.

Five Years of Experimental Warming Increases the Biodiversity and Productivity of Phytoplankton.

Phytoplankton are key components of aquatic ecosystems, fixing CO2 from the atmosphere through photosynthesis and supporting secondary production, yet relatively little is known about how future global warming might alter their biodiversity and associated ecosystem functioning. Here, we explore how the structure, function, and biodiversity of a planktonic metacommunity was altered after five years of experimental warming. Our outdoor mesocosm experiment was open to natural dispersal from the regional species pool, allowing us to explore the effects of experimental warming in the context of metacommunity dynamics. Warming of 4°C led to a 67% increase in the species richness of the phytoplankton, more evenly-distributed abundance, and higher rates of gross primary productivity. Warming elevated productivity indirectly, by increasing the biodiversity and biomass of the local phytoplankton communities. Warming also systematically shifted the taxonomic and functional trait composition of the phytoplankton, favoring large, colonial, inedible phytoplankton taxa, suggesting stronger top-down control, mediated by zooplankton grazing played an important role. Overall, our findings suggest that temperature can modulate species coexistence, and through such mechanisms, global warming could, in some cases, increase the species richness and productivity of phytoplankton communities.

Reconciling the temperature dependence of respiration across timescales and ecosystem types.

Ecosystem respiration is the biotic conversion of organic carbon to carbon dioxide by all of the organisms in an ecosystem, including both consumers and primary producers. Respiration exhibits an exponential temperature dependence at the subcellular and individual levels, but at the ecosystem level respiration can be modified by many variables including community abundance and biomass, which vary substantially among ecosystems. Despite its importance for predicting the responses of the biosphere to climate change, it is as yet unknown whether the temperature dependence of ecosystem respiration varies systematically between aquatic and terrestrial environments. Here we use the largest database of respiratory measurements yet compiled to show that the sensitivity of ecosystem respiration to seasonal changes in temperature is remarkably similar for diverse environments encompassing lakes, rivers, estuaries, the open ocean and forested and non-forested terrestrial ecosystems, with an average activation energy similar to that of the respiratory complex (approximately 0.65 electronvolts (eV)). By contrast, annual ecosystem respiration shows a substantially greater temperature dependence across aquatic (approximately 0.65 eV) versus terrestrial ecosystems (approximately 0.32 eV) that span broad geographic gradients in temperature. Using a model derived from metabolic theory, these findings can be reconciled by similarities in the biochemical kinetics of metabolism at the subcellular level, and fundamental differences in the importance of other variables besides temperature­such as primary productivity and allochthonous carbon inputs­on the structure of aquatic and terrestrial biota at the community level.

Weighting and indirect effects identify keystone species in food webs.

Species extinctions are accelerating globally, yet the mechanisms that maintain local biodiversity remain poorly understood. The extinction of species that feed on or are fed on by many others (i.e. 'hubs') has traditionally been thought to cause the greatest threat of further biodiversity loss. Very little attention has been paid to the strength of those feeding links (i.e. link weight) and the prevalence of indirect interactions. Here, we used a dynamical model based on empirical energy budget data to assess changes in ecosystem stability after simulating the loss of species according to various extinction scenarios. Link weight and/or indirect effects had stronger effects on food-web stability than the simple removal of 'hubs', demonstrating that both quantitative fluxes and species dissipating their effects across many links should be of great concern in biodiversity conservation, and the potential for 'hubs' to act as keystone species may have been exaggerated to date.

Temperature effects on fish production across a natural thermal gradient.

Global warming is widely predicted to reduce the biomass production of top predators, or even result in species loss. Several exceptions to this expectation have been identified, however, and it is vital that we understand the underlying mechanisms if we are to improve our ability to predict future trends. Here, we used a natural warming experiment in Iceland and quantitative theoretical predictions to investigate the success of brown trout as top predators across a stream temperature gradient (4-25 °C). Brown trout are at the northern limit of their geographic distribution in this system, with ambient stream temperatures below their optimum for maximal growth, and above it in the warmest streams. A five-month mark-recapture study revealed that population abundance, biomass, growth rate, and production of trout all increased with stream temperature. We identified two mechanisms that contributed to these responses: (1) trout became more selective in their diet as stream temperature increased, feeding higher in the food web and increasing in trophic position; and (2) trophic transfer through the food web was more efficient in the warmer streams. We found little evidence to support a third potential mechanism: that external subsidies would play a more important role in the diet of trout with increasing stream temperature. Resource availability was also amplified through the trophic levels with warming, as predicted by metabolic theory in nutrient-replete systems. These results highlight circumstances in which top predators can thrive in warmer environments and contribute to our knowledge of warming impacts on natural communities and ecosystem functioning.

Higher biodiversity is required to sustain multiple ecosystem processes across temperature regimes.

Biodiversity loss is occurring rapidly worldwide, yet it is uncertain whether few or many species are required to sustain ecosystem functioning in the face of environmental change. The importance of biodiversity might be enhanced when multiple ecosystem processes (termed multifunctionality) and environmental contexts are considered, yet no studies have quantified this explicitly to date. We measured five key processes and their combined multifunctionality at three temperatures (5, 10 and 15 °C) in freshwater aquaria containing different animal assemblages (1-4 benthic macroinvertebrate species). For single processes, biodiversity effects were weak and were best predicted by additive-based models, i.e. polyculture performances represented the sum of their monoculture parts. There were, however, significant effects of biodiversity on multifunctionality at the low and the high (but not the intermediate) temperature. Variation in the contribution of species to processes across temperatures meant that greater biodiversity was required to sustain multifunctionality across different temperatures than was the case for single processes. This suggests that previous studies might have underestimated the importance of biodiversity in sustaining ecosystem functioning in a changing environment.

Climate change and geothermal ecosystems: natural laboratories, sentinel systems, and future refugia.

Understanding and predicting how global warming affects the structure and functioning of natural ecosystems is a key challenge of the 21st century. Isolated laboratory and field experiments testing global change hypotheses have been criticized for being too small-scale and overly simplistic, whereas surveys are inferential and often confound temperature with other drivers. Research that utilizes natural thermal gradients offers a more promising approach and geothermal ecosystems in particular, which span a range of temperatures within a single biogeographic area, allow us to take the laboratory into nature rather than vice versa. By isolating temperature from other drivers, its ecological effects can be quantified without any loss of realism, and transient and equilibrial responses can be measured in the same system across scales that are not feasible using other empirical methods. Embedding manipulative experiments within geothermal gradients is an especially powerful approach, informing us to what extent small-scale experiments can predict the future behaviour of real ecosystems. Geothermal areas also act as sentinel systems by tracking responses of ecological networks to warming and helping to maintain ecosystem functioning in a changing landscape by providing sources of organisms that are preadapted to different climatic conditions. Here, we highlight the emerging use of geothermal systems in climate change research, identify novel research avenues, and assess their roles for catalysing our understanding of ecological and evolutionary responses to global warming.

Down-the-drain pathways for fipronil and imidacloprid applied as spot-on parasiticides to dogs: Estimating aquatic pollution.

Fipronil and imidacloprid have been widely detected in UK surface waters in recent years, often at concentrations that ecotoxicological studies have shown can harm aquatic life. Down-the-drain (DTD) passage of pet flea and tick treatments are being implicated as an important source, with many of the UK's 22 million cats and dogs receiving routine, year-round preventative doses containing these parasiticides. The UK Water Industry's 3rd Chemical Investigation Programme (UKWIR CIP3) has confirmed wastewater as a major entry pathway for these chemicals into surface waters, but the routes by which they enter the wastewater system remain unclear. We addressed this knowledge gap by conducting the first quantification of DTD emissions from 98 dogs treated with spot-on ectoparasiticides containing fipronil or imidacloprid, through bathing, bed washing and washing of owners' hands. Both chemicals were detected in 100 % of washoff samples, with bathing accounting for the largest emissions per event (up to 16.8 % of applied imidacloprid and 24.5 % of applied fipronil). Modelled to account for the frequency of emitting activities, owner handwashing was identified as the largest source of DTD emissions from the population overall, with handwash emissions occurring for at least 28 days following product application and an estimated 4.9 % of imidacloprid and 3.1 % of fipronil applied in dog spot-ons passing down-the-drain via this route. The normalised daily per capita emissions for all routes combined were 8.7 µg/person/day for imidacloprid and 2.1 µg/person/day for fipronil, equivalent to 20-40 % of the daily per capita load in wastewater, as estimated from UKWIR CIP3 data. Within the current international regulatory framework adhered to by the UK, the environmental exposure of veterinary medicines intended for use in small companion animals is assumed to be low, and DTD pathways are not considered. We recommend a systematic review of regulations and practices to address this overlooked pollution pathway.

High-throughput characterization of bacterial responses to complex mixtures of chemical pollutants.

Our understanding of how microbes respond to micropollutants, such as pesticides, is almost wholly based on single-species responses to individual chemicals. However, in natural environments, microbes experience multiple pollutants simultaneously. Here we perform a matrix of multi-stressor experiments by assaying the growth of model and non-model strains of bacteria in all 255 combinations of 8 chemical stressors (antibiotics, herbicides, fungicides and pesticides). We found that bacterial strains responded in different ways to stressor mixtures, which could not be predicted simply from their phylogenetic relatedness. Increasingly complex chemical mixtures were both more likely to negatively impact bacterial growth in monoculture and more likely to reveal net interactive effects. A mixed co-culture of strains proved more resilient to increasingly complex mixtures and revealed fewer interactions in the growth response. These results show predictability in microbial population responses to chemical stressors and could increase the utility of next-generation eco-toxicological assays.

Regional impacts of warming on biodiversity and biomass in high latitude stream ecosystems across the Northern Hemisphere.

Warming can have profound impacts on ecological communities. However, explorations of how differences in biogeography and productivity might reshape the effect of warming have been limited to theoretical or proxy-based approaches: for instance, studies of latitudinal temperature gradients are often conflated with other drivers (e.g., species richness). Here, we overcome these limitations by using local geothermal temperature gradients across multiple high-latitude stream ecosystems. Each suite of streams (6-11 warmed by 1-15°C above ambient) is set within one of five regions (37 streams total); because the heating comes from the bedrock and is not confounded by changes in chemistry, we can isolate the effect of temperature. We found a negative overall relationship between diatom and invertebrate species richness and temperature, but the strength of the relationship varied regionally, declining more strongly in regions with low terrestrial productivity. Total invertebrate biomass increased with temperature in all regions. The latter pattern combined with the former suggests that the increased biomass of tolerant species might compensate for the loss of sensitive species. Our results show that the impact of warming can be dependent on regional conditions, demonstrating that local variation should be included in future climate projections rather than simply assuming universal relationships.

Diatoms can be an important exception to temperature-size rules at species and community levels of organization.

Climate warming has been linked to an apparent general decrease in body sizes of ectotherms, both across and within taxa, especially in aquatic systems. Smaller body size in warmer geographical regions has also been widely observed. Since body size is a fundamental determinant of many biological attributes, climate-warming-related changes in size could ripple across multiple levels of ecological organization. Some recent studies have questioned the ubiquity of temperature-size rules, however, and certain widespread and abundant taxa, such as diatoms, may be important exceptions. We tested the hypothesis that diatoms are smaller at warmer temperatures using a system of geothermally heated streams. There was no consistent relationship between size and temperature at either the population or community level. These field data provide important counterexamples to both James' and Bergmann's temperature-size rules, respectively, undermining the widely held assumption that warming favours the small. This study provides compelling new evidence that diatoms are an important exception to temperature-size rules for three reasons: (i) we use many more species than prior work; (ii) we examine both community and species levels of organization simultaneously; (iii) we work in a natural system with a wide temperature gradient but minimal variation in other factors, to achieve robust tests of hypotheses without relying on laboratory setups, which have limited realism. In addition, we show that interspecific effects were a bigger contributor to whole-community size differences, and are probably more ecologically important than more commonly studied intraspecific effects. These findings highlight the need for multispecies approaches in future studies of climate warming and body size.

Grazing and detritivory in 20 stream food webs across a broad pH gradient.

Acidity is a major driving variable in the ecology of fresh waters, and we sought to quantify macroecological patterns in stream food webs across a wide pH gradient. We postulated that a few generalist herbivore-detritivores would dominate the invertebrate assemblage at low pH, with more specialists grazers at high pH. We also expected a switch towards algae in the diet of all primary consumers as the pH increased. For 20 stream food webs across the British Isles, spanning pH 5.0-8.4 (the acid sites being at least partially culturally acidified), we characterised basal resources and primary consumers, using both gut contents analysis and stable isotopes to study resource use by the latter. We found considerable species turnover across the pH gradient, with generalist herbivore-detritivores dominating the primary consumer assemblage at low pH and maintaining grazing. These were joined or replaced at higher pH by a suite of specialist grazers, while many taxa that persisted across the pH gradient broadened the range of algae consumed as acidity declined and increased their ingestion of biofilm, whose nutritional quality was higher than that of coarse detritus. There was thus an increased overall reliance on algae at higher pH, both by generalist herbivore-detritivores and due to the presence of specialist grazers, although detritus was important even in non-acidic streams. Both the ability of acid-tolerant, herbivore-detritivores to exploit both autochthonous and allochthonous food and the low nutritional value of basal resources might render chemically recovering systems resistant to invasion by the specialist grazers and help explain the sluggish ecological recovery of fresh waters whose water chemistry has ameliorated.

Warming indirectly simplifies food webs through effects on apex predators.

Warming alters ecosystems through direct physiological effects on organisms and indirect effects via biotic interactions, but their relative impacts in the wild are unknown due to the difficulty in warming natural environments. Here we bridge this gap by embedding manipulative field experiments within a natural stream temperature gradient to test whether warming and apex fish predators have interactive effects on freshwater ecosystems. Fish exerted cascading effects on algal production and microbial decomposition via both green and brown pathways in the food web, but only under warming. Neither temperature nor the presence of fish altered food web structure alone, but connectance and mean trophic level declined as consumer species were lost when both drivers acted together. A mechanistic model indicates that this temperature-induced trophic cascade is determined primarily by altered interactions, which cautions against extrapolating the impacts of warming from reductionist approaches that do not consider the wider food web.