Mechanistic population models for ecological risk assessment and decision support: The importance of good conceptual model diagrams.

The use of mechanistic population models as research and decision-support tools in ecology and ecological risk assessment (ERA) is increasing. This growth has been facilitated by advances in technology, allowing the simulation of more complex systems, as well as by standardized approaches for model development, documentation, and evaluation. Mechanistic population models are particularly useful for simulating complex systems, but the required model complexity can make them challenging to communicate. Conceptual diagrams that summarize key model elements, as well as elements that were considered but not included, can facilitate communication and understanding of models and increase their acceptance as decision-support tools. Currently, however, there are no consistent standards for creating or presenting conceptual model diagrams (CMDs), and both terminology and content vary widely. Here, we argue that greater consistency in CMD development and presentation is an important component of good modeling practice, and we provide recommendations, examples, and a free web app (pop-cmd.com) for achieving this for population models used for decision support in ERAs. Integr Environ Assess Manag 2024;20:1566-1574. © 2023 SETAC.

Moving beyond Risk Quotients: Advancing Ecological Risk Assessment to Reflect Better, More Robust and Relevant Methods.

Under standard guidance for conducting Ecological Risk Assessments (ERAs), the risks of chemical exposure to diverse organisms are most often based on deterministic point estimates evaluated against safety-factor-based levels of concern (LOCs). While the science and guidance for mechanistic effect models (e.g., demographic, population, and agent-based) have long been demonstrated to provide more ecologically relevant effect endpoints upon which risk can be evaluated, their application in ERAs has been limited, particularly in the US. This special issue highlights the state of the science in effect modeling for ERAs through demonstrated application of the recently published Population modeling Guidance, Use, Interpretation, and Development for ERA (Pop-GUIDE). We introduce this issue with a perspective on why it is critical to move past the current application of deterministic endpoints and LOCs. We demonstrate how the current, widely used approaches contain extensive uncertainty that could be reduced considerably by applying models that account for species life histories and other important endogenous and exogenous factors critical to species sustainability. We emphasize that it is long past time to incorporate better, more robust, and ecologically relevant effect models into ERAs, particularly for chronic risk determination. The papers in this special issue demonstrate how mechanistic models that follow Pop-GUIDE better inform ERAs compared to the current standard practice.

Population modeling to inform management and recovery efforts for lake sturgeon, Acipenser fulvescens.

Lake sturgeon (Acipenser fulvescens) populations have significantly declined across their historic range, in large part due to anthropogenic impacts that have likely been exacerbated by the life-history traits of this slow-growing and long-lived species. We developed a population model to explore how Contaminants of Emerging Concern (CECs) impact lake sturgeon populations. We explored how different physiological modes of action (pMoAs) of CECs impacted population abundance and recovery and how different simulated management actions could enable recovery. We first estimated the impacts on population abundance and recovery by comparing the trajectory of an unexposed population to a population that had been exposed to a CEC with a specific pMoA after the end of the exposure. We then predicted how different management actions would impact population recovery by comparing the trajectories of an unexposed population to an exposed population for which a management action started at a fixed time without discontinuation of the exposure. Our results predicted that the individual-level pMoA of CECs has an important impact on population-level effects because different stressor's pMoA impacts the life-history traits of sturgeon differently. For example, the feeding and reproduction pMoAs caused the strongest and weakest population declines, respectively. For the same reason, pMoA also impacted recovery. For example, recovery was delayed when the pMoA was growth, maintenance, or feeding, but it was immediate when the pMoA was reproduction. We found that management actions that increased the egg survival rate or the stocking of fingerlings resulted in faster and stronger recovery than management actions that increased the juvenile or adult survival rate. This result occurred because the first two management actions immediately impacted recruitment, whereas the impact was delayed for the last two. Finally, there was greater potential for recovery when management action targeted eggs and fingerlings because these life stages have lower natural survival rates. Integr Environ Assess Manag 2022;18:1597-1608. © 2022 Society of Environmental Toxicology & Chemistry (SETAC). This article has been contributed to by US Government employees and their work is in the public domain in the USA.

Long-term effects of sediment-associated silver nanoparticles and silver nitrate on the deposit-feeding polychaete Capitella teleta.

Aquatic sediments are predicted to be an important sink for released silver nanoparticles (AgNPs). Knowing the long-term effects of AgNPs on benthic deposit-feeders is therefore an important step towards assessing their potential environmental risks. The aim of this study was to examine the effects on survival, growth and reproduction of the deposit-feeding polychaete Capitella teleta exposed for ten weeks to sediment-associated un-coated AgNPs or silver nitrate (AgNO3). C. teleta exhibited tolerance towards exposure to both AgNPs and AgNO3. Significant effects were observed for percentage of pairs that reproduced as well as worm growth after eight weeks, but the effects did not show a clear concentration- or Ag type-dependent pattern. Further investigations of long-term effects of un-coated AgNPs in additional sediment-dwelling organisms are needed and should involve comparisons to coated AgNPs.

Probable role of Cutibacterium acnes in the gut of the polychaete Capitella teleta.

Capitella teleta, a marine polychaete that feeds on a refractory diet consisting of sediment, was shown to contain unique gut microbiota comprised of microbial functional groups involved in fermentation. Results of our previous studies showed that C. teleta's core gut microbiota were dominated by propionibacteria, and that these bacteria were more abundant in worms than in sediment and feces. In order to test the hypothesis that the worm nutritionally benefits from its gut microbiota, we identified, and genetically and biochemically characterized Cutibacterium acnes strains (formerly Propionibacterium acnes) that were isolated from the gut of C. teleta. Here we show that 13 worm-isolated Cutibacterium acnes strains primarily belonged to phylotype group IB, likely as a clonal population. We also provide evidence that all tested strains produced propionate and vitamin B12, which are essential host-requiring microbial metabolites. The presence of C. acnes in C. teleta was not unique to our worm culture and was also found in those obtained from geographically distant laboratories located in the U.S. and Europe. Moreover, populations of worm gut-associated C. acnes increased following antibiotic treatment. Collectively, results of this study demonstrated that C. acnes is a member of the worm's core functional microbiota and is likely selectively favored by the physiology and chemistry of the host gut environment. To our knowledge, this is the first report of the presence of C. acnes in the C. teleta gut. Our data strongly suggest that C. acnes, a bacterium previously studied as an opportunistic pathogen, can likely act as a symbiont in C. teleta providing the host essential nutrients for survival, growth, and reproduction.

A simulation-based evaluation of management actions to reduce the risk of contaminants of emerging concern (CECs) to walleye in the Great Lakes Basin.

Contaminants of emerging concern (CECs) are ubiquitous, present in complex chemical mixtures, and represent a threat to the Great Lake ecosystem. Mitigation strategies are needed to protect populations of key species, but knowledge about ecological and biological effects of CECs at the population level are limited. In this study, we combined laboratory data on CEC effects at the individual-level with in-situ CEC concentration data in a walleye (Sander vitreus) population model to simulate the effectiveness of different CEC mitigation strategies in the Maumee River and Lake Erie. We compared the effectiveness of moderate mitigation (50% reduction in exposure level) of an entire watershed versus intensive mitigation (reduction of exposure to a level that does not affect walleye) of single river sites for three CEC mixture scenarios (agricultural, urban, and combined). We also explored the impact of hypothetical chemical toxicokinetics (the time course of chemicals in walleye) on the relative effectiveness of the mitigation strategies. Our results suggest that when CECs impact fecundity, single-site mitigation is more effective when it focuses on spawning sites and nearby downstream sites that are substantially impaired. Our simulations also suggest that chemical toxicokinetics are important when evaluating single-site mitigation strategies, but that population characteristics, such as stage-specific mortality rate, are more important when evaluating watershed mitigation strategies. Results can be used to guide fisheries management, such as choosing habitat restoration sites, and identify key knowledge gaps that direct future research and monitoring.

Mechanistic Effect Modeling of Earthworms in the Context of Pesticide Risk Assessment: Synthesis of the FORESEE Workshop.

Earthworms are important ecosystem engineers, and assessment of the risk of plant protection products toward them is part of the European environmental risk assessment (ERA). In the current ERA scheme, exposure and effects are represented simplistically and are not well integrated, resulting in uncertainty when the results are applied to ecosystems. Modeling offers a powerful tool to integrate the effects observed in lower tier laboratory studies with the environmental conditions under which exposure is expected in the field. This paper provides a summary of the (In)Field Organism Risk modEling by coupling Soil Exposure and Effect (FORESEE) Workshop held 28-30 January 2020 in Düsseldorf, Germany. This workshop focused on toxicokinetic-toxicodynamic (TKTD) and population modeling of earthworms in the context of ERA. The goal was to bring together scientists from different stakeholder groups to discuss the current state of soil invertebrate modeling and to explore how earthworm modeling could be applied to risk assessments, in particular how the different model outputs can be used in the tiered ERA approach. In support of these goals, the workshop aimed at addressing the requirements and concerns of the different stakeholder groups to support further model development. The modeling approach included 4 submodules to cover the most relevant processes for earthworm risk assessment: environment, behavior (feeding, vertical movement), TKTD, and population. Four workgroups examined different aspects of the model with relevance for risk assessment, earthworm ecology, uptake routes, and cross-species extrapolation and model testing. Here, we present the perspectives of each workgroup and highlight how the collaborative effort of participants from multidisciplinary backgrounds helped to establish common ground. In addition, we provide a list of recommendations for how earthworm TKTD modeling could address some of the uncertainties in current risk assessments for plant protection products. Integr Environ Assess Manag 2021;17:352-363. © 2020 SETAC.

A Review of Key Features and Their Implementation in Unstructured, Structured, and Agent-Based Population Models for Ecological Risk Assessment.

Population models can provide valuable tools for ecological risk assessment (ERA). A growing amount of work on model development and documentation is now available to guide modelers and risk assessors to address different ERA questions. However, there remain misconceptions about population models for ERA, and communication between regulators and modelers can still be hindered by a lack of clarity in the underlying formalism, implementation, and complexity of different model types. In particular, there is confusion about differences among types of models and the implications of including or ignoring interactions of organisms with each other and their environment. In this review, we provide an overview of the key features represented in population models of relevance for ERA, which include density dependence, spatial heterogeneity, external drivers, stochasticity, life-history traits, behavior, energetics, and how exposure and effects are integrated in the models. We differentiate 3 broadly defined population model types (unstructured, structured, and agent-based) and explain how they can represent these key features. Depending on the ERA context, some model features will be more important than others, and this can inform model type choice, how features are implemented, and possibly the collection of additional data. We show that nearly all features can be included irrespective of formalization, but some features are more or less easily incorporated in certain model types. We also analyze how the key features have been used in published population models implemented as unstructured, structured, and agent-based models. The overall aim of this review is to increase confidence and understanding by model users and evaluators when considering the potential and adequacy of population models for use in ERA. Integr Environ Assess Manag 2021;17:521-540. © 2020 SETAC.

Temperature dependence of population responses to competition and metabolic stress: An agent-based model to inform ecological risk assessment in a changing climate.

Understanding the interactions among multiple stressors is a crucial issue for ecological risk assessment and ecosystem management. However, it is often impractical, or impossible, to collect empirical data concerning all the interactions at any scale because the type of interaction differs across species and levels of biological organization. We applied an agent-based model to simulate the effects of a hypothetical chemical stressor and inter-specific competition (both alone and together) on greenback cutthroat trout (GCT), a listed species under the US Endangered Species Act, in two temperature scenarios. The trout life cycle is modeled using the Dynamic Energy Budget theory. The chemical stressor is represented by a reduction in ingestion efficiency, and competition is implemented by introducing a population of brown trout. Results show that chemical exposure is the major stressor in the colder temperature scenario, whereas competition mostly affected the GCT population in the warmer environment. Moreover, the effects of the stressors at the individual level were not predictive of the type of interactions between stressors (additive, antagonistic, synergistic) at the population level, which differed between the two-temperature scenarios. We conclude that mechanistic models can help to identify generalities about interactions among environmental and stressor properties, create in-silico experiments to provide different scenarios for conservation purposes, and explore multiple-exposure consequences at higher levels of biological organization. In this way they can provide useful tools for improving ecological risk assessment and informing management decisions.

Bioturbation by the marine polychaete Capitella teleta alters the sediment microbial community by ingestion and defecation of sediment particles.

Deposit-feeding benthic invertebrates are known to modify sediment structure and impact microbial processes associated with biogeochemical cycles in marine sedimentary environments. Despite this, however, there is limited information on how sediment ingestion and defecation by marine benthos alters microbial community structure and function in sediments. In the current study, we used high-throughput sequencing data of 16S rRNA genes obtained from a previous microcosm study to examine how sediment processing by the marine polychaete Capitella teleta specifically affects sediment microbiota. Here we show that both sediment ingestion and defecation by C. teleta significantly alters overall microbial community structure and function. Sediment processing by C. teleta resulted in significant enrichment of sediment microbial communities involved in sulfur and carbon cycling in worm fecal pellets. Moreover, C. teleta's microbiota was predominantly comprised of bacterial functional groups involved in fermentation, relative to microbiota found outside of the host. Collectively, results of this study indicate that C. teleta has the ability to alter microbial biogeochemical cycles in the benthic sedimentary environment by altering microbial assemblages in the worm gut, and in the sediment ingested and defecated by worms as they feed on sediment particles. In this sense, C. teleta plays an important role as an ecosystem engineer and in shaping nutrient cycling in the benthic environment.

Divergent density feedback control of migratory predator recovery following sex-biased perturbations.

Uncertainty in risks posed by emerging stressors such as synthetic hormones impedes conservation efforts for threatened vertebrate populations. Synthetic hormones often induce sex-biased perturbations in exposed animals by disrupting gonad development and early life-history stage transitions, potentially diminishing per capita reproductive output of depleted populations and, in turn, being manifest as Allee effects. We use a spatially explicit biophysical model to evaluate how sex-biased perturbation in life-history traits of individuals (maternal investment in egg production and male-skewed sex allocation in offspring) modulates density feedback control of year-class strength and recovery trajectories of a long-lived, migratory fish-shovelnose sturgeon (Scaphirhynchus platorynchus)-under spatially and temporally dynamic synthetic androgen exposure and habitat conditions. Simulations show that reduced efficiency of maternal investment in gonad development prolonged maturation time, increased the probability of skipped spawning, and, in turn, shrunk spawner abundance, weakening year-class strength. However, positive density feedback disappeared (no Allee effect) once the exposure ceased. By contrast, responses to the demographic perturbation manifested as strong positive density feedback; an abrupt shift in year-class strength and spawner abundance followed after more than two decades owing to persistent negative population growth (a strong Allee effect), reaching an alternative state without any sign of recovery. When combined with the energetic perturbation, positive density feedback of the demographic perturbation was dampened as extended maturation time reduced the frequency of producing male-biased offspring, allowing the population to maintain positive growth rate (a weak Allee effect) and gradually recover. The emergent patterns in long-term population projections illustrate that sex-biased perturbation in life-history traits can interactively regulate the strength of density feedback in depleted populations such as Scaphirhynchus sturgeon to further diminish reproductive capacity and abundance, posing increasingly greater conservation challenges in chemically altered riverscapes.

Lack of evidence for the role of gut microbiota in PAH biodegradation by the polychaete Capitella teleta.

Capitella teleta is a marine sediment-feeding polychaete known to degrade various polycyclic aromatic hydrocarbons (PAHs) and reported to possess genes involved in PAH transformation, such as those in the P450 cytochrome superfamily. Previous research focusing on biodegradation of PAHs by C. teleta demonstrated that these worms are effective biodegraders, but overlooked the possible role of its gut microbiota in facilitating PAH metabolism. Recently, C. teleta's microbiome was characterized and found to contain several bacterial genera known to contain PAH-degrading members, including Acinetobacter, Thalassotalea, and Achromobacter. Despite this, however, no data have thus far been presented demonstrating the role of C. teleta's gut microbiota in PAH degradation. The present study was designed to more conclusively determine the presence of PAH-degrading bacteria in worm digestive tracts and to more clearly distinguish the relative roles of worm versus gut-microbial metabolism in the removal of PAH from sediment. To do this, we manipulated marine sediment microorganisms and worm gut microbiota by autoclaving and antibiotic treatment, respectively. Our results showed that no fluoranthene degradation occurred in microcosms in the absence of worms. More importantly, there was no significant difference in fluoranthene degradation between antibiotic-treated and non-treated worms. We also found no evidence of fluoranthene degradation using resting cells of gut microbes of C. teleta, and we were unable to isolate fluoranthene-degrading bacterial strains from enrichments of polychaete gut contents, despite multiple attempts. Gut microbiota in worms treated with antibiotics recovered, through bidirectional transfer, between worms and sediment after 2 weeks of microcosm incubation, and gut microbes appear to be required for the survival and growth of C. teleta. Our results build on previous studies suggesting that C. teleta itself is primarily responsible for the metabolism of fluoranthene in ingested sediment. We hypothesize that C. teleta's core microbiota, which includes members of Propionibacterium as the most abundant genus, likely aid worms in obtaining key nutrients (e.g., vitamins) from its sediment diet.

Similar individual-level responses to stressors have different population-level consequences among closely related species of trout.

In this paper, we applied an individual-based model to study the population-level impacts of sub-lethal stressors affecting the metabolic pathways of three closely related trout species: Oncorhynchus mykiss (rainbow trout, RT), Salmo trutta (brown trout, BT) and Oncorhynchus calrki stomias (greenback cutthroat trout, GCT). Both RT and BT are well-studied species, and the former is widely used as a standard cold-water test species. These species are known to outcompete GCT, which is listed as threatened under the US Endangered Species Act. Our goal was to understand the extent to which stressor effects, which are often measured at the individual level, on taxonomically-related (i.e., surrogate) species can be informative of impacts on population dynamics in species that cannot be tested (e.g., listed species). When comparing stressor effects among species, we found that individual-level responses to each stressor were qualitatively comparable. Individual lengths and number of eggs decreased by similar percentages with respect to baseline, even if small quantitative differences were present depending on the physiological mode of action of the stressor. Individual-level effects in GCT were slightly greater when ingestion efficiency decreased, whereas effects in GCT and RT were greater when maintenance costs increased, and effects in BT were slightly greater when costs of growth increased. In contrast, results at the population level differed markedly among species with GCT the most impacted by sub-lethal stress effects on individual metabolism. Our findings suggest that using non-listed species to assess the risks of stressors to listed species populations may be misleading, even if the species are closely related and show similar individual-level responses. Mechanistic population models that incorporate species life history and ecology can improve inter-species extrapolation of stressor effects.

Predicting impacts of chemicals from organisms to ecosystem service delivery: A case study of insecticide impacts on a freshwater lake.

Assessing and managing risks of anthropogenic activities to ecological systems is necessary to ensure sustained delivery of ecosystem services for future generations. Ecological models provide a means of quantitatively linking measured risk assessment endpoints with protection goals, by integrating potential chemical effects with species life history, ecological interactions, environmental drivers and other potential stressors. Here we demonstrate how an ecosystem modeling approach can be used to quantify insecticide-induced impacts on ecosystem services provided by a lake from toxicity data for organism-level endpoints. We used a publicly available aquatic ecosystem model AQUATOX that integrates environmental fate of chemicals and their impacts on food webs in aquatic environments. By simulating a range of exposure patterns, we illustrated how exposure to a hypothetical insecticide could affect aquatic species populations (e.g., recreational fish abundance) and environmental properties (e.g., water clarity) that would in turn affect delivery of ecosystem services. Different results were observed for different species of fish, thus the decision to manage the use of the insecticide for ecosystem services derived by anglers depends upon the favored species of fish. In our hypothetical shallow reservoir, water clarity was mostly driven by changes in food web dynamics, specifically the presence of zooplankton. In contrast to the complex response by fishing value, water clarity increased with reduced insecticide use, which produced a monotonic increase in value by waders and swimmers. Our study clearly showed the importance of considering nonlinear ecosystem feedbacks where the presence of insecticide changed the modeled food-web dynamics in unexpected ways. Our study highlights one of the main advantages of using ecological models for risk assessment, namely the ability to generalize to meaningful levels of organization and to facilitate quantitative comparisons among alternative scenarios and associated trade-offs among them while explicitly accounting for different groups of beneficiaries.

The deposit feeder Capitella teleta has a unique and relatively complex microbiome likely supporting its ability to degrade pollutants.

Capitella teleta is a sediment-dwelling marine polychaete that is often found in high densities in association with organic matter and pollutants. While C. teleta has been reported to transform a variety of aromatic hydrocarbons, the mechanisms by which degradation occurs are unknown. Moreover, there is continuing debate on the role of host and microbiota in degradation activity. The aims of this study were to characterize the gut microbiome of C. teleta and to identify microbiota that could potentially play a role in degradation of organic matter and aromatic hydrocarbons. Sequencing analysis of the 16S rRNA genes from the intestinal tracts of adult worms revealed a unique microbiome that was distinct from that of the worm's sediment food source and fecal pellets. About 66% of the 775 identified OTUs from the C. teleta gut microbiome were found to be unique to the worm and displayed high inter-individual variability. The gut microbiome was dominated by members of the genera Arcobacter, Pseudoalteromonas, Methylobacterium, and Propionibacterium. Functional analyses of microbiota revealed that hydrocarbon treatment led to a proliferation of gene classes involved in chemoheterotrophy and aromatic compound degradation. Of the 18 most abundant taxa identified, 50% were members of genera containing hydrocarbon (PAH)-degrading members, including Acinetobacter, Thalassotalea, and Achromobacter. Data obtained in this study will be useful to understand the biology of this marine polychaete and to elucidate the role that gut bacteria play in worm catabolism and the transformation of sediment organic pollutants.

Predicting impacts of chemicals from organisms to ecosystem service delivery: A case study of endocrine disruptor effects on trout.

We demonstrate how mechanistic modeling can be used to predict whether and how biological responses to chemicals at (sub)organismal levels in model species (i.e., what we typically measure) translate into impacts on ecosystem service delivery (i.e., what we care about). We consider a hypothetical case study of two species of trout, brown trout (Salmo trutta; BT) and greenback cutthroat trout (Oncorhynchus clarkii stomias; GCT). These hypothetical populations live in a high-altitude river system and are exposed to human-derived estrogen (17α­ethinyl estradiol, EE2), which is the bioactive estrogen in many contraceptives. We use the individual-based model inSTREAM to explore how seasonally varying concentrations of EE2 could influence male spawning and sperm quality. Resulting impacts on trout recruitment and the consequences of such for anglers and for the continued viability of populations of GCT (the state fish of Colorado) are explored. inSTREAM incorporates seasonally varying river flow and temperature, fishing pressure, the influence of EE2 on species-specific demography, and inter-specific competition. The model facilitates quantitative exploration of the relative importance of endocrine disruption and inter-species competition on trout population dynamics. Simulations predicted constant EE2 loading to have more impacts on GCT than BT. However, increasing removal of BT by anglers can enhance the persistence of GCT and offset some of the negative effects of EE2. We demonstrate how models that quantitatively link impacts of chemicals and other stressors on individual survival, growth, and reproduction to consequences for populations and ecosystem service delivery, can be coupled with ecosystem service valuation. The approach facilitates interpretation of toxicity data in an ecological context and gives beneficiaries of ecosystem services a more explicit role in management decisions. Although challenges remain, this type of approach may be particularly helpful for site-specific risk assessments and those in which tradeoffs and synergies among ecosystem services need to be considered.

Applying ecosystem services for pre-market environmental risk assessments of regulated stressors.

Ecosystem services (ES) are the benefits that people obtain from ecosystems. Investigating the environment through an ES framework has gained wide acceptance in the international scientific community and is applied by policymakers to protect biodiversity and safeguard the sustainability of ecosystems. This approach can enhance the ecological and societal relevance of pre-market/prospective environmental risk assessments (ERAs) of regulated stressors by: (1) informing the derivation of operational protection goals; (2) enabling the integration of environmental and human health risk assessments; (3) facilitating horizontal integration of policies and regulations; (4) leading to more comprehensive and consistent environmental protection; (5) articulating the utility of, and trade-offs involved in, environmental decisions; and (6) enhancing the transparency of risk assessment results and the decisions based upon them. Realisation of these advantages will require challenges that impede acceptance of an ES approach to be overcome. Particularly, there is concern that, if biodiversity only matters to the extent that it benefits humans, the intrinsic value of nature is ignored. Moreover, our understanding of linkages among ecological components and the processes that ultimately deliver ES is incomplete, valuing ES is complex, and there is no standard ES lexicon and limited familiarity with the approach. To help overcome these challenges, we encourage: (1) further research to establish biodiversity-ES relationships; (2) the development of approaches that (i) quantitatively translate responses to chemical stressors by organisms and groups of organisms to ES delivery across different spatial and temporal scales, (ii) measure cultural ES and ease their integration into ES valuations, and (iii) appropriately value changes in ES delivery so that trade-offs among different management options can be assessed; (3) the establishment of a standard ES lexicon; and (4) building capacity in ES science and how to apply ES to ERAs. These development needs should not prevent movement towards implementation of an ES approach in ERAs, as the advantages we perceive of using this approach render it more than worthwhile to tackle those challenges. Society and the environment stand to benefit from this shift in how we conduct the ERA of regulated stressors.

Adverse impacts of hypoxia on aquatic invertebrates: A meta-analysis.

Hypoxia in aquatic ecosystems is often a result of anthropogenic activities, such as increased nutrient loading, originating from agriculture or urbanization, as well as global warming. Aquatic invertebrates are especially important in ecosystems due to their central role in secondary production and in dynamics of food webs. To better understand impacts of oxygen availability on key physiological processes in invertebrates, we conducted a literature search and synthesized the findings of published studies. We found 55 studies that quantified impacts of hypoxia on feeding, growth, reproduction and respiration rates in 54 different aquatic invertebrate species. We applied non-linear regression models which took into account phylogenetic correlation in the data set. Fitting Michaelis-Menten models, we found that there were differences in how different processes responded to a decline in oxygen availability. Respiration rates were halved at highest oxygen concentration (6.44 mg O2/L), followed by reproductive (3.66 mg O2/L), growth (1.77 mg O2/L) and, finally, feeding rates (0.77 mg O2/L). Our findings confirm observations that reproduction is highly sensitive as organisms quickly reduce their reproductive output when exposed to stressful conditions. As long as they have sufficient reserves, organisms continue growing even under stressful conditions, and we confirmed that growth was not very sensitive to a decline in oxygen availability. We discuss potential impacts of global warming on oxygen availability and demand for aquatic macroinvertebrates. Given that oxygen availability is declining in many ecosystems, we can expect that organismal responses will be increasingly compromised with potential consequences for ecosystems and the services they deliver.