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Predicting the synergy of multiple stress effects

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ABSTRACT

Toxicants and other, non-chemical environmental stressors contribute to the global biodiversity crisis. Examples include the loss of bees and the reduction of aquatic biodiversity. Although non-compliance with regulations might be contributing, the widespread existence of these impacts suggests that for example the current approach of pesticide risk assessment fails to protect biodiversity when multiple stressors concurrently affect organisms. To quantify such multiple stress effects, we analysed all applicable aquatic studies and found that the presence of environmental stressors increases individual sensitivity to toxicants (pesticides, trace metals) by a factor of up to 100. To predict this dependence, we developed the “Stress Addition Model” (SAM). With the SAM, we assume that each individual has a general stress capacity towards all types of specific stress that should not be exhausted. Experimental stress levels are transferred into general stress levels of the SAM using the stress-related mortality as a common link. These general stress levels of independent stressors are additive, with the sum determining the total stress exerted on a population. With this approach, we provide a tool that quantitatively predicts the highly synergistic direct effects of independent stressor combinations.

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Increase of toxicant sensitivity in relation to additional environmental stress – (A) Stress Addition Model, SAM; (B) Traditional approaches from mixture toxicity. The x-axis shows the magnitude of environmental stress, expressed as mortality without toxicant exposure. The y-axis shows the increase in toxicant sensitivity. Observations: Points indicate aquatic vertebrate and invertebrate studies with 23 pairs of concentration-response relationships, including 6 different environmental stressors, 5 toxicants and 10 species. (A) Modelling by the SAM: Lines indicate the modelled increase in toxicant sensitivity for the LC10 (LC10/LC10*) and the LC50 (LC50/LC50*) in relation to the environmental stress. (B) Modelling by traditional approaches from mixture toxicity: Lines indicate the modelled increase in toxicant sensitivity using the extended approach of concentration addition (CA, blue and red solid lines), and effect addition (EA, blue and red dashed lines). Details on the experimental studies see Table S1 and Figure S1. The grey shaded area represents the results of the model based on the standard error of the average normalized concentration-response curve (see Methods).
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f1: Increase of toxicant sensitivity in relation to additional environmental stress – (A) Stress Addition Model, SAM; (B) Traditional approaches from mixture toxicity. The x-axis shows the magnitude of environmental stress, expressed as mortality without toxicant exposure. The y-axis shows the increase in toxicant sensitivity. Observations: Points indicate aquatic vertebrate and invertebrate studies with 23 pairs of concentration-response relationships, including 6 different environmental stressors, 5 toxicants and 10 species. (A) Modelling by the SAM: Lines indicate the modelled increase in toxicant sensitivity for the LC10 (LC10/LC10*) and the LC50 (LC50/LC50*) in relation to the environmental stress. (B) Modelling by traditional approaches from mixture toxicity: Lines indicate the modelled increase in toxicant sensitivity using the extended approach of concentration addition (CA, blue and red solid lines), and effect addition (EA, blue and red dashed lines). Details on the experimental studies see Table S1 and Figure S1. The grey shaded area represents the results of the model based on the standard error of the average normalized concentration-response curve (see Methods).

Mentions: We aimed to empirically identify the impact of additional environmental stress on the toxicant sensitivity of individuals. For this, we reviewed all published studies of the combined impact of environmental stressors and toxicants that met our inclusion criteria (see Methods, Table S1). This meta-analysis revealed that additional environmental stress strongly increases the toxicant sensitivity of individuals (Fig. 1). The increase of toxicant sensitivity is thereby quantified as the shift of the lethal concentration from the concentration-response-relationship of the toxicant alone (LCx) compared to the concentration-response relationship of the toxicant under environmental stress (LCx*). For high-effect levels of a toxicant (50% mortality; LC50/LC50*), the presence of environmental stressors increases individual sensitivity to toxicants by a factor of up to 10, whereas for low-effect levels of a toxicant (10% mortality; LC10/LC10*), the presence of environmental stressors increases individual sensitivity to toxicants by a factor of up to 100. It is also remarkable that even levels of environmental stress without a measurable mortality effect may considerably increase the sensitivity to toxicants (Fig. 1). The relationship between environmental stress and sensitivity to toxicants could be approximated by a linear regression (LC50/LC50* r2 = 0.65, p < 0.001; LC10/LC10* r2 = 0.63, p < 0.001). This close relationship is particularly surprising because the analysis included 6 different environmental stressors, 5 toxicants with 3 different modes of action and 10 different vertebrate and invertebrate species (Table S1). For the first time, this approach systematically quantified the increase of toxicant sensitivity in relation to environmental stress for several investigations across various stressors and species.


Predicting the synergy of multiple stress effects
Increase of toxicant sensitivity in relation to additional environmental stress – (A) Stress Addition Model, SAM; (B) Traditional approaches from mixture toxicity. The x-axis shows the magnitude of environmental stress, expressed as mortality without toxicant exposure. The y-axis shows the increase in toxicant sensitivity. Observations: Points indicate aquatic vertebrate and invertebrate studies with 23 pairs of concentration-response relationships, including 6 different environmental stressors, 5 toxicants and 10 species. (A) Modelling by the SAM: Lines indicate the modelled increase in toxicant sensitivity for the LC10 (LC10/LC10*) and the LC50 (LC50/LC50*) in relation to the environmental stress. (B) Modelling by traditional approaches from mixture toxicity: Lines indicate the modelled increase in toxicant sensitivity using the extended approach of concentration addition (CA, blue and red solid lines), and effect addition (EA, blue and red dashed lines). Details on the experimental studies see Table S1 and Figure S1. The grey shaded area represents the results of the model based on the standard error of the average normalized concentration-response curve (see Methods).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5017025&req=5

f1: Increase of toxicant sensitivity in relation to additional environmental stress – (A) Stress Addition Model, SAM; (B) Traditional approaches from mixture toxicity. The x-axis shows the magnitude of environmental stress, expressed as mortality without toxicant exposure. The y-axis shows the increase in toxicant sensitivity. Observations: Points indicate aquatic vertebrate and invertebrate studies with 23 pairs of concentration-response relationships, including 6 different environmental stressors, 5 toxicants and 10 species. (A) Modelling by the SAM: Lines indicate the modelled increase in toxicant sensitivity for the LC10 (LC10/LC10*) and the LC50 (LC50/LC50*) in relation to the environmental stress. (B) Modelling by traditional approaches from mixture toxicity: Lines indicate the modelled increase in toxicant sensitivity using the extended approach of concentration addition (CA, blue and red solid lines), and effect addition (EA, blue and red dashed lines). Details on the experimental studies see Table S1 and Figure S1. The grey shaded area represents the results of the model based on the standard error of the average normalized concentration-response curve (see Methods).
Mentions: We aimed to empirically identify the impact of additional environmental stress on the toxicant sensitivity of individuals. For this, we reviewed all published studies of the combined impact of environmental stressors and toxicants that met our inclusion criteria (see Methods, Table S1). This meta-analysis revealed that additional environmental stress strongly increases the toxicant sensitivity of individuals (Fig. 1). The increase of toxicant sensitivity is thereby quantified as the shift of the lethal concentration from the concentration-response-relationship of the toxicant alone (LCx) compared to the concentration-response relationship of the toxicant under environmental stress (LCx*). For high-effect levels of a toxicant (50% mortality; LC50/LC50*), the presence of environmental stressors increases individual sensitivity to toxicants by a factor of up to 10, whereas for low-effect levels of a toxicant (10% mortality; LC10/LC10*), the presence of environmental stressors increases individual sensitivity to toxicants by a factor of up to 100. It is also remarkable that even levels of environmental stress without a measurable mortality effect may considerably increase the sensitivity to toxicants (Fig. 1). The relationship between environmental stress and sensitivity to toxicants could be approximated by a linear regression (LC50/LC50* r2 = 0.65, p < 0.001; LC10/LC10* r2 = 0.63, p < 0.001). This close relationship is particularly surprising because the analysis included 6 different environmental stressors, 5 toxicants with 3 different modes of action and 10 different vertebrate and invertebrate species (Table S1). For the first time, this approach systematically quantified the increase of toxicant sensitivity in relation to environmental stress for several investigations across various stressors and species.

View Article: PubMed Central - PubMed

ABSTRACT

Toxicants and other, non-chemical environmental stressors contribute to the global biodiversity crisis. Examples include the loss of bees and the reduction of aquatic biodiversity. Although non-compliance with regulations might be contributing, the widespread existence of these impacts suggests that for example the current approach of pesticide risk assessment fails to protect biodiversity when multiple stressors concurrently affect organisms. To quantify such multiple stress effects, we analysed all applicable aquatic studies and found that the presence of environmental stressors increases individual sensitivity to toxicants (pesticides, trace metals) by a factor of up to 100. To predict this dependence, we developed the &ldquo;Stress Addition Model&rdquo; (SAM). With the SAM, we assume that each individual has a general stress capacity towards all types of specific stress that should not be exhausted. Experimental stress levels are transferred into general stress levels of the SAM using the stress-related mortality as a common link. These general stress levels of independent stressors are additive, with the sum determining the total stress exerted on a population. With this approach, we provide a tool that quantitatively predicts the highly synergistic direct effects of independent stressor combinations.

No MeSH data available.


Related in: MedlinePlus