Bioenergetics‐adverse outcome pathway: Linking organismal and suborganismal energetic endpoints to adverse outcomes

Abstract

Adverse outcome pathways (AOPs) link toxicity across levels of biological organization, and thereby facilitate the development of suborganismal responses predictive of whole‐organism toxicity and provide the mechanistic information necessary for science‐based extrapolation to population‐level effects. Thus far AOPs have characterized various acute and chronic toxicity pathways; however, the potential for AOPs to explicitly characterize indirect, energy‐mediated effects from toxicants has yet to be fully explored. Indeed, although exposure to contaminants can alter an organism's energy budget, energetic endpoints are rarely incorporated into ecological risk assessment because there is not an integrative framework for linking energetic effects to organismal endpoints relevant to risk assessment (e.g., survival, reproduction, growth). In the present analysis, we developed a generalized bioenergetics‐AOP in an effort to make better use of energetic endpoints in risk assessment, specifically exposure scenarios that generate an energetic burden to organisms. To evaluate empirical support for a bioenergetics‐AOP, we analyzed published data for links between energetic endpoints across levels of biological organization. We found correlations between 1) cellular energy allocation and whole‐animal growth, and 2) metabolic rate and scope for growth. Moreover, we reviewed literature linking energy availability to nontraditional toxicological endpoints (e.g., locomotor performance), and found evidence that toxicants impair aerobic performance and activity. We conclude by highlighting current knowledge gaps that should be addressed to develop specific bioenergetics‐AOPs. Environ Toxicol Chem 2019;38:27–45. © 2018 SETAC

Negative bioenergetic responses to pesticides in damselfly larvae are more likely when it is hotter and when temperatures fluctuate

“…The CEA reflects the net energy budget that is available for an organism by taking the ratio of energy stored in reserve molecules (energy available, Ea) over the energy that is consumed (energy consumption, Ec) (De Coen and Janssen, 2003). The CEA can be used as an indicator for effects on higher levels of biological organization as it has been shown to positively correlate with organismal growth rate (Goodchild et al, 2019;Verslycke et al, 2004). CEA has been often used as a biomarker for toxicant stress (e.g.…”

“…Following Sokolova (2013) we also tested whether bioenergetic responses contributed to the observed toxicity patterns in terms of mortality and growth reduction that we reported in the companion study. Our hypothesis was that treatment groups with a lower CEA to show a higher mortality and a lower growth rate (cfr Goodchild et al, 2019)…”

Application of Biomarker Tools Using Bivalve Models Toward the Development of Adverse Outcome Pathways for Contaminants of Emerging Concern

“…Bioenergetic endpoints and biomarkers associated with energy depletion and reallocation in bivalves exposed to contaminant stress have been documented in xenobiotic studies (Sokolova et al 2012). Therefore, integration of models such as the dynamic energy budget (DEB) approach (Kooijman 2000) into the AOP framework can provide linkages between energetic effects and apical/organismal endpoints such as growth, survival, and reproduction in bivalves (Goodchild et al 2019). Such use of bioenergetic modeling with bivalves (Steeves et al 2018) in conjunction with toxicity data sets (Jager and Selck 2011) can support the development of improved predictive approaches in ecological management and risk assessment.…”

Lower bioenergetic costs but similar immune responsiveness under a heat wave in urban compared to rural damselflies

“…Another set of key fitness‐related physiological variables are bioenergetic variables (Goodchild, Simpson, Minghetti, & DuRant, 2019; Sokolova, 2013). Energy availability and energy consumption are especially important, as these provide information about the “energy gain and loss” balance (Sokolova, 2013).…”