## 4.4.4. Multistress - abiotic

Author: Martina Vijver

Reviewers: Kees van Gestel, Michiel Kraak, Martin Holmstrup

Learning objectives:

You should be able to

- relate stress to the ecological niche concept
- list abiotic factors that may alter the toxic effects of chemicals on organisms, and indicate if these abiotic factors decrease or increase the toxic effects of chemicals on organisms

Key words: Stress, ecological niche concept, multistress, chemical-abiotic interactions

Introduction: stress related to the ecological niche concept

The concept of stress can be defined at various levels of biological organization, from biochemistry to species fitness, ultimately leading to changes in community structure and ecosystem functioning. Yet, stress is most often studied in the context of individual organisms. The concept of stress is not absolute and can only be defined with reference to the normal range of ecological functioning. This is the case when organisms are within their range of tolerance (so-called ecological amplitude) or within their ecological niche, which describes the match of a species to specific environmental conditions. Applying this concept to stress allows it to be defined as a condition evoked in an organism by one or more environmental factors that bring the organism near or over the edges of its ecological niche (Van Straalen, 2003), see Figure 1.

Figure 1. Schematic illustration of the ecological amplitude or niche-based (bell shaped curve) definition of stress. Stress arises when an environmental factor increases from point 1 to point 2 (red line) and the species is forced outside its ecological niche. By definition, the organism cannot grow and reproduce outside this niche, but it may survive there temporarily, if it can return in time to its niche (blue line). If the borders of the niche are extended through adaptation, then this specific state of the environmental factor does not result in stress anymore and the performance of the species falls within the normal operating range at that condition (green line). Redrawn from Van Straalen (2003) by Wilma IJzerman.

Multistress is subsequently defined as a situation in which an organism is exposed both to a toxicant and to stressful environmental conditions (see section Multistress – Introduction and definitions). This includes chemical-abiotic interactions, chemical-biotic interactions (see section Multistress – chemical – biotic interactions) as well as combinations of these. In general, organisms living under conditions close to their environmental tolerance limits appear to be more vulnerable to additional chemical stress. The opposite also holds: if organisms are stressed due to exposure to elevated levels of contaminants, their ability to cope with sub-optimal environmental conditions is reduced.

Chemical-abiotic interactions

Temperature. One of the predominant environmental factors altering toxic effects obviously is temperature. For poikilothermic (cold-blooded) organisms, increases in temperature lead to an increase in activity, which may affect both the uptake and the effects of chemicals. In a review by Heugens et al. (2001), studies reporting the effect chemicals on aquatic organisms in combination with abiotic factors like temperature, nutritional state and salinity were discussed. Generally, toxic effects increased with increasing temperature. Dependent on the effect parameter studied, the differences in toxic effects between laboratory and relevant field temperatures ranged from a factor of 2 to 130.

Also freezing temperatures may interfere with chemical effects as was shown in another influential review of Holmstrup et al. (2010). Membrane damage is mentioned as an explanation for the synergistic interaction between combinations of metals and temperatures below zero.

Food. Food availability may have a strong effect on the sensitivity of organisms to chemicals (see section Multistress – chemical – biotic interactions). In general decreasing food or nutrient levels increased toxicity, resulting in differences in toxicity between laboratory and relevant field situations ranging from a factor of 1.2 to 10 (Heugens et al., 2001). Yet, way higher differences in toxic effects related to food levels have been reported as well: Experiments performed with daphnids in cages that were placed in outdoor mesocosm ditches (see sections on Cosm studies and In situ bioassays) showed stunning differences in sensitivity to the insecticide thiacloprid. Under conditions of low to ambient nutrient concentrations, the observed toxicity, expressed as the lowest observed effect concentration (LOEC) for growth and reproduction occurred at thiacloprid concentrations that were 2500-fold lower than laboratory-derived LOEC values. Contrary to the low nutrient treatment, such altered toxicity was often not observed under nutrient-enriched conditions (Barmentlo et al submitted). The difference was likely attributable to the increased primary production that allowed for compensatory feeding and perhaps also reduced the bioavailability of the insecticide. Similar results were observed for sub-lethal endpoints measured on the damselfly species Ischnura elegans, for which the response to thiacloprid exposure strongly depended on food availability and quality. Damselfies that were feeding on natural resources were significantly more affected than those that were offered high quality artificial food (Barmentlo et al submitted).

Salinity. The influence of salinity on toxicity is less clear (Heugens et al. 2001). If salinity pushes the organism towards its niche boundaries, it will worsen the toxic effects that it is experiencing. In case that a specific salinity fits in the ecological niche of the organism, processes affecting exposure will predominantly determine the stress it will experience. This for instance means that metal toxicity decreases with increasing salinity, as it is strongly affected by the competition of ions (see section on Metal speciation). The toxic effect induced by organophosphate insecticides however, increases with increasing salinity. For other chemicals, no clear relationship between toxicity and salinity was observed. A salinity increase from freshwater to marine water decreased toxicity by a factor of 2.1 (Heugens et al. 2001). However, as less extreme salinity changes are more relevant under field conditions, the change in toxicity is probably much smaller.

pH. Many organisms have a species-specific range of pH levels at which they function optimally. At pH values outside the optimal range, organisms may show reduced reproduction and growth, in extreme cases even reduced survival. In some cases, the effects of pH may be indirect, as pH may also have an important impact on exposure of organisms to toxicants. This is especially the case for metals and ionizable chemicals: metal speciation, but also the form in which ionizable chemicals occur in the environment and therefore their bioavailability, is highly dependent on pH (see sections on Metal speciation and Ionogenic organic chemicals). An example of the interaction between pH and metal effects was shown by Crommentuijn et al. (1997), who observed a reduced control reproduction of the springtail Folsomia candida, but also the lowest cadmium toxicity at a soil pHKCl 7.0 compared to pHKCl 3.1-5.7.

Drought. In soil, the moisture content (see section on Soil) is an important factor, since drought is often limiting the suitability of the soil as a habitat for organisms. Holmstrup et al. (2010), reviewing the literature, concluded that chemicals interfering with the drought tolerance of soil organisms, e.g. by affecting the functioning of membranes or the accumulation of sugars, may exacerbate the effects of drought. Earthworms are breathing through the skin and can only survive in moist soils, and the eggs of springtails can only survive at a relative air humidity close to 100%. This makes these organisms especially sensitive to drought, which may be enhanced by exposure to chemicals like metals, polycyclic aromatic hydrocarbon or surfactants (Holmstrup et al., 2010).

Many different abiotic conditions, such as oxygen levels, light, turbidity, and organic matter content, can push organisms towards the boundaries of their niche, but we will not discuss all stressors in this book.

Multistress in environmental risk assessment

In environmental risk assessment, differences between stress-induced effects as determined in the laboratory under standardized optimal conditions with a single toxicant and the effects induced by multiple stressors are taken into account by applying an uncertainty factor. Yet, the choice for uncertainty factors is based on little ecological evidence. In 2001, Heugens already argued for obtaining uncertainty factors that sufficiently protect natural systems without being overprotective. Van Straalen (2003) echoed this and in current research the question is still raised if enough understanding has been gained to make accurate laboratory-to-field extrapolations. It remains a challenge to predict toxicant-induced effects on species and even on communities while accounting for variable and suboptimal environmental conditions, even though these conditions are common aspects of natural ecosystems (see for instance the section on Eco-epidemiology).

References

Barmentlo, S.H., Vriend, L.M, van Grunsven, R.H.A., Vijver, M.G. (submitted). Evidence that neonicotinoids contribute to damselfly decline.

Crommentuijn, T., Doornekamp, A., Van Gestel, C.A.M. (1997). Bioavailability and ecological effects of cadmium on Folsomia candida (Willem) in an artificial soil substrate as influenced by pH and organic matter. Applied Soil Ecology 5, 261-271.

Heugens, E.H., Hendriks, A.J., Dekker, T., Van Straalen, N.M., Admiraal, W. (2001). A review of the effects of multiple stressors on aquatic organisms and analysis of uncertainty factors for use in risk assessment. Critical Reviews in Toxicology 31, 247-84.

Holmstrup, M., Bindesbøl, A.M., Oostingh, G.J., Duschl, A., Scheil, V., Köhler, H.R., Loureiro, S., Soares, A.M.V.M., Ferreira, A.L.G., Kienle, C., Gerhardt, A., Laskowski, R., Kramarz, P.E., Bayley, M., Svendsen, C., Spurgeon, D.J. (2010). Review Interactions between effects of environmental chemicals and natural stressors: A review. Science of the Total Environment 408, 3746–3762.

Van Straalen, N.M. (2003). Ecotoxicology becomes stress ecology Environmental Science and Technology 37, 324A-330A.