2017 Progress Report: A Bioenergetics-Based Approach to Understanding and Predicting Individual- to Community-Level Ecological Effects of Manufactured Chemicals

EPA Grant Number: R835800
Title: A Bioenergetics-Based Approach to Understanding and Predicting Individual- to Community-Level Ecological Effects of Manufactured Chemicals
Investigators: J. Salice, Christopher
Institution: Towson University
EPA Project Officer: Lasat, Mitch
Project Period: September 1, 2015 through August 31, 2018 (Extended to August 31, 2019)
Project Period Covered by this Report: January 1, 2017 through December 15,2017
Project Amount: $374,510
RFA: Systems-Based Research for Evaluating Ecological Impacts of Manufactured Chemicals (2014) RFA Text |  Recipients Lists
Research Category: Ecological Indicators/Assessment/Restoration , Ecosystems , Safer Chemicals

Objective:

A fundamental goal in ecotoxicology and ecological risk assessment (ERA) is to predict the frequency and magnitude of adverse ecological effects resulting from chemical contaminants. While there is a considerable volume of research generated on the effects of a wide variety of manufactured chemicals on ecologically relevant receptors, the vast majority of studies are focused at levels of biological organization that are most conducive to empirical approaches – the individual and lower. Paradoxically, the levels of biological organization that are most relevant to environmental health and societal value are at the population level and higher (communities and ecosystems). The overarching objective of the proposed research is to develop a bioenergetics-based Adverse Outcome Pathway framework that can translate from individual-level to population- and community-level effects of manufactured chemicals.

Progress Summary:

Specific Aim 1: Establish bioenergetics-based responses and associated mathematical models (e.g., Dynamic Energy Budget (DEB), Von Bertelanffy growth model) of individual study species exposed to PFOS and pyraclostrobin for 2-4 week exposures, which are representative of relatively low-cost, standardized toxicity tests.

  • Endpoints: Life history traits, cellular energy assimilation, metabolic rate, feeding rate, fatty acid profiles – growth rate as a key endpoint.
  • Models: Single species bioenergetics (DEB) and growth models.

Summary Specific Aim 1 Progress: We have successfully conducted a series of relatively short duration toxicity studies to explore the effects of pyraclostrobin and perfluorooctane sulfonate (PFOS) on Daphnia magna and/or Lymnaea stagnalis. Our research has shown that pyraclostrobin is more toxic than PFOS and we have what we think is a well-developed understanding of pyraclostrobin toxicity to our aquatic test species. After extensive toxicity testing in both L. stagnalis and D. magna, the more relevant exposure and effect scenario for pyraclostrobin appears to be related to short duration, acute toxicity.

As mentioned, PFOS is less toxic than pyraclostrobin but interestingly appears to exert toxicity in subtle ways and after long duration exposures. As an example, PFOS increased the variability in population size in Daphnia which then translates to an increase in extinction risk. These results were obtained from a novel study design that we developed where cohorts of Daphnia are exposed and the laboratory populations are followed through time. This method yields insights into effects of chemicals on population dynamics and implicitly include density-dependent.

Additionally, we have explored the impact of the “resource environment” on toxicity and have generated some very interesting and somewhat counterintuitive results. Two papers on this subject have been published with a third in draft. Moreover, we have conducted a series of acute toxicity studies with Daphnia and pyraclostrobin over a series of resource levels and have shown that as resource levels increase, pyraclostrobin toxicity decreases.

We have measured lipid profiles as a bioenergetics endpoint in Daphnia under different food regimes. Additionally, we have measured lipid profiles in chironomids from streams representing an urban (stressed) to rural (less stressed) environment. We have preliminary evidence that lipid profiles yield some insight into toxicological effects although we now think that this is a subtle endpoint and that longer-term data is needed to draw meaningful inference. We acquired the means to measure metabolic rate in small organisms (Daphnia) and our preliminary studies show that exposure to pyraclostrobin appears to cause an increase in metabolic rate which preliminarily confirms our hypothesis.

Specific Aim 2: Establish bioenergetics-based responses, life-history effects and population-level effects of individual study species exposed to PFOS and pyraclostrobin using a Life Table Response Experiment study design (full life cycle exposure). 

  • Endpoints: Same as Specific Aim 1 plus population-level endpoints (population growth rate, estimated abundance, stable stage distribution)
  • Models: Individual-based and cohort-based population models

Summary Specific Aim 2 Progress: Full life-cycle, cohort-based study designs for Daphnia have now become a staple of our laboratory studies. This design involves initiating a “laboratory population” with a few individuals and allowing them to grow and reproduce with no culling for at least 40 days. This yields a very predictable population cycle of growth, peak, decline and stable phases. We have used this design to test toxicity of PFOS and pyraclostrobin to Daphnia magna. In our most recent work, MS student Tim Woo, explored the implications of the timing of pyraclostrobin pulses on population responses.

We had previously developed a dynamic energy budget – individual based model (DEB-IBM) for Daphnia that was spatially explicit and included crowding as a factor important to Daphnia population dynamics. The model produces output that closely matches our experimental population data provided; we have resource-specific toxicity values. This effort is nearing publication-ready.

Specific Aim 3: Establish bioenergetics-based responses, life history effects and population-level effects of individual study species exposed to PFOS and pyraclostrobin in addition to the presence of conspecific competitors and predators.

  • Endpoints: Same as Specific Aim 1 plus modified life history based on species interactions (competition coefficients; predator-prey coefficients)
  • Models: Density dependent, resource based population models; Modified population models that include mortality from predation

Summary Specific Aim 3 Progress: We have completed studies in which we have combined L. stagnalis and D. magna. In this scenario, the nature of the interaction is energetic facilitation to D. magna via L. stagnalis. Specifically, L. stagnalis “liberates” sources of energy (lettuce) making it available to D. magna. This is a relatively under studied form of species interaction but one that is likely common and potentially important. Also, our population study design for D. magna includes density-dependent effects and hence, intra-species competition. Our DEB-IBM also captures these dynamic well and illustrates one important attribute of IBMs – properties and dynamics of populations can emerge from the interactions and behaviors of individuals. To support the D. magna + L. stagnalis studies, we have developed a model that links DEB models for Daphnia and snails and yields excellent agreement with study results.

We have initiated studies with Daphnia involving predatory damselflies. The goal is to work towards generating more complex ecological scenarios and to develop models that can predict the outcome of complex ecological interactions. To simplify what can be a very challenging and complex ecological scenario, our model output will still focus on predicting Daphnia population dynamics. Once we have data from complex systems, however, we will explore other modeling platforms and endpoints. Our results thus far with damselflies have yielded excellent results for consumption of Daphnia and acute toxicity studies have shown that the species is much less sensitive to pyraclostrobin than Daphnia. These results can be used in our model to predict effects of predators and chemicals on Daphnia. One interesting factor to consider, however, will be the structure of the environment as the availability of refugia for Daphnia will influence stress from predators. These experiments will be forthcoming and are the focus of spring 2018 research efforts.

Future Activities:

The next phases of the planned research address more complex experimental designs that include multiple species. Currently, we have been exploring the use of damselflies as predators of D. magna. They are extremely effective predators with size-specific consumption rates. The goal will be to further develop and test our DEB-IBM and population models to determine if they still hold predictive capability under more complex ecological scenarios. We intend to manipulate the resource environment, the predator environment and the structural environment of simulated aquatic communities. These experimental communities will be exposed to pulses of pyraclostrobin and constant levels of road salt. Road salt is an important issue for freshwater organisms in the Mid-Atlantic.

Once data are in hand, we will retrospectively explore model predictive capability and work to develop and test new or existing models. We hypothesize, like others have, that many factors can influence the ecological consequences of toxicant exposure. We are hopeful, however, that significant insights into the ecological effects can be obtained from understanding a few key drivers of effects. We hypothesize that in complex environments, effects of chemicals on D. magna will be significantly influenced by the resource environment, the predator environment and the physical structure of the habitat (refugia).

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Journal Articles on this Report : 2 Displayed | Download in RIS Format

Other project views: All 17 publications 2 publications in selected types All 2 journal articles
Type Citation Project Document Sources
Journal Article Reategui-Zirena EG, Fidder BN, Olson AD, Dawson DE, Bilbo TR, Salice CJ. Transgenerational endpoints provide increased sensitivity and insight into multigenerational responses of Lymnaea stagnalis exposed to cadmium. Environmental Pollution 2017;224:572-580. R835800 (2016)
R835800 (2017)
  • Abstract from PubMed
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  • Abstract: ScienceDirect-Abstract
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  • Other: ScienceDirect-Full Text PDF
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  • Journal Article Rohr JR, Salice CJ, Nisbet RM. The pros and cons of ecological risk assessment based on data from different levels of biological organization. Critical Reviews in Toxicology 2016;46(9):756-784. R835800 (2016)
    R835800 (2017)
    R835188 (Final)
    R835797 (2015)
    R835797 (2016)
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  • Abstract from PubMed
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  • Full-text: University of South Florida-Full Text PDF
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  • Abstract: Taylor & Francis-Abstract
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  • Progress and Final Reports:

    Original Abstract
  • 2016 Progress Report
  • 2018