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 (17α‑ethinyl estradiol, EE2), which is the bioactive estrogen in many contraceptives. We use the individual based model in STREAM 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. in STREAM 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 amore 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 trade offs and synergies among ecosystem services need to be considered

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 (17α‑ethinyl estradiol, EE2), which is the bioactive estrogen in many contraceptives. We use the individual based model in STREAM 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. in STREAM 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 amore 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 trade offs and synergies among ecosystem services need to be considered

Pairwise Comparisons for Differences in Total Summer Biomass between Scenario and Baseline.

<p>Pairwise comparisons of total biomass (g) of trout in summer for forest harvest (FH), climate change (CC), and combined (FH + CC) scenarios compared to baseline in modeled streams, including Gus Creek, Pothole Creek, Rock Creek, and Upper Mainstem (UM). Values of summer biomass by year were averaged for five replicate simulations and were analyzed using Wilcoxon signed rank test (V) with continuity correction resulting in a pseudomedian of difference between scenario and baseline (Δ) for the 1^st harvest period, 2^nd harvest period, and the entire study period. Scenarios include manipulations of stream temperature and flow regimes (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0135334#sec002" target="_blank">Methods</a> for details). Significant p-values in bold (alpha ≤ 0.05) represent increasing or decreasing magnitudes in comparison to baseline.</p><p>Pairwise Comparisons for Differences in Total Summer Biomass between Scenario and Baseline.</p

Local Variability Mediates Vulnerability of Trout Populations to Land Use and Climate Change

<div><p>Land use and climate change occur simultaneously around the globe. Fully understanding their separate and combined effects requires a mechanistic understanding at the local scale where their effects are ultimately realized. Here we applied an individual-based model of fish population dynamics to evaluate the role of local stream variability in modifying responses of Coastal Cutthroat Trout (<i>Oncorhynchus clarkii clarkii</i>) to scenarios simulating identical changes in temperature and stream flows linked to forest harvest, climate change, and their combined effects over six decades. We parameterized the model for four neighboring streams located in a forested headwater catchment in northwestern Oregon, USA with multi-year, daily measurements of stream temperature, flow, and turbidity (2007–2011), and field measurements of both instream habitat structure and three years of annual trout population estimates. Model simulations revealed that variability in habitat conditions among streams (depth, available habitat) mediated the effects of forest harvest and climate change. Net effects for most simulated trout responses were different from or less than the sum of their separate scenarios. In some cases, forest harvest countered the effects of climate change through increased summer flow. Climate change most strongly influenced trout (earlier fry emergence, reductions in biomass of older trout, increased biomass of young-of-year), but these changes did not consistently translate into reductions in biomass over time. Forest harvest, in contrast, produced fewer and less consistent responses in trout. Earlier fry emergence driven by climate change was the most consistent simulated response, whereas survival, growth, and biomass were inconsistent. Overall our findings indicate a host of local processes can strongly influence how populations respond to broad scale effects of land use and climate change.</p></div

Influence of Flow and Temperature on Trout Biomass within each Scenario.

<p>Boxplots of mean total summer biomass (g) of trout in Gus Creek, Pothole Creek, Rock Creek, and Upper Mainstem (UM) from five replicate simulations over the entire study period. Each boxplot incorporates 63 data points of the mean of every year’s summer biomass per scenario. Gray boxes represent pairwise comparisons of the influence of flow (Q), stream temperature (T), and both (Q+T) within each scenario of forest harvest (FH) and climate change (CC). Baseline and the combined scenarios (FH+CC) are shown for reference. Scenarios include manipulations of stream temperature and flow regimes (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0135334#sec002" target="_blank">methods</a> narrative for detail). Significant pairwise differences are shown by a horizontal black line (P < 0.05). Significant differences between baseline and each scenario are noted. The point above or below each boxplot corresponds to the 5^th and 95^th percentile.</p

Differences in Total Summer Biomass of Trout between Scenarios and Baseline.

<p>Difference in mean total summer biomass (g) from the five replicated simulations over time for each scenario of forest harvest (FH), climate change (CC), and their combined effects (FH+CC) compared to baseline, in Gus Creek, Pothole Creek, Rock Creek, and Upper Mainstem (UM). Scenarios include manipulations of stream temperature and flow regimes (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0135334#sec002" target="_blank">methods</a> narrative for detail). Only significant trends (P < 0.05) for the entire study period have been numerically shown with the slope of the trend (g/decade).</p

Trends in Fry Emergence of Trout across Scenarios.

<p>DOY from five replicate simulations when median number of modeled fry had emerged over time in Gus Creek, Pothole Creek, Rock Creek, and Upper Mainstem (UM). Scenarios include manipulations of stream temperature and flow regimes (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0135334#sec002" target="_blank">methods</a> narrative for detail). Only significant trends (P < 0.05) over time are listed and include the slope of the trend (days per decade). Negative values represent early fry emergence. Gaps in data are due to years with no fry emergence because model thresholds for spawning, egg development, or emergence were not met.</p

A Framework for Predicting Impacts on Ecosystem Services From (Sub)Organismal Responses to Chemicals

Protection of ecosystem services is increasingly emphasized as a risk-assessment goal, but there are wide gaps between current ecological risk-assessment endpoints and potential effects on services provided by ecosystems. The authors present a framework that links common ecotoxicological endpoints to chemical impacts on populations and communities and the ecosystem services that they provide. This framework builds on considerable advances in mechanistic effects models designed to span multiple levels of biological organization and account for various types of biological interactions and feedbacks. For illustration, the authors introduce 2 case studies that employ well-developed and validated mechanistic effects models: the inSTREAM individual-based model for fish populations and the AQUATOX ecosystem model. They also show how dynamic energy budget theory can provide a common currency for interpreting organism-level toxicity. They suggest that a framework based on mechanistic models that predict impacts on ecosystem services resulting from chemical exposure, combined with economic valuation, can provide a useful approach for informing environmental management. The authors highlight the potential benefits of using this framework as well as the challenges that will need to be addressed in future work

A framework for predicting impacts on ecosystem services from (sub)organismal responses to chemicals

Protection of ecosystem services is increasingly emphasized as a risk-assessment goal, but there are wide gaps between current ecological risk-assessment endpoints and potential effects on services provided by ecosystems. The authors present a framework that links common ecotoxicological endpoints to chemical impacts on populations and communities and the ecosystem services that they provide. This framework builds on considerable advances in mechanistic effects models designed to span multiple levels of biological organization and account for various types of biological interactions and feedbacks. For illustration, the authors introduce 2 case studies that employ well-developed and validated mechanistic effects models: the inSTREAM individual-based model for fish populations and the AQUATOX ecosystem model. They also show how dynamic energy budget theory can provide a common currency for interpreting organism-level toxicity. They suggest that a framework based on mechanistic models that predict impacts on ecosystem services resulting from chemical exposure, combined with economic valuation, can provide a useful approach for informing environmental management. The authors highlight the potential benefits of using this framework as well as the challenges that will need to be addressed in future work. Environ Toxicol Chem 2017;36:845-859. © 2017 SETAC

Representation of Key Processes in inSTREAM.

<p>We highlight how the daily time series inputs of stream temperature, flow, and turbidity drive individual growth and survival and hence population dynamics including responses of fry emergence and biomass. A more detailed explanation of inSTREAM can be found in [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0135334#pone.0135334.ref020" target="_blank">20</a>–<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0135334#pone.0135334.ref021" target="_blank">21</a>].</p