## 4.4.3. Multistress - biotic

Authors: Marjolein Van Ginneken and Lieven Bervoets

Reviewers: Michiel Kraak and Martin Holmstrup

Learning objectives:

You should be able to

- define biotic stress and to give three examples.
- explain how biotic stressors can change the toxicity of chemicals
- explain how chemicals can change the way organisms react to biotic stressors

Keywords: Multistress, chemical-biotic interactions, stressor interactions, bioavailability, behavior, energy trade-off

Introduction

Generally, organisms have to cope with the joint presence of chemical and natural stressors. Both biotic and abiotic stressors can affect the chemicals’ bioavailability and toxicokinetics. Additionally, they can influence the behavior and physiology of organisms, which could result in higher or lower toxic effects. Vice versa, chemicals can alter the way organisms react to natural stressors.

By studying the effects of multiple stressors, we can identify potential synergistic, additive or antagonistic interactions, which are essential to adequately assess the risk of chemicals in nature. Relyea (2003), for instance, found that apparently safe concentrations of carbaryl can become deadly to some amphibian species when combined with predator cues. This section focuses on biotic stress, which can be defined as stress caused by living organisms and includes predation, competition, population density, food availability, pathogens and parasitism. It will describe how biotic stressors and chemicals act and interact.

Types of biotic stressors

Biotic stressors can have direct and indirect effects on organisms. For example, predators can change food web structures by consuming their prey and thus altering prey abundance and can indirectly affect prey growth and development as well, by inducing energetically-costly defense mechanisms. Also behaviors like (foraging) activity can be decreased and even morphological changes can be induced. For example, Daphnia pulex can develop neck spines when they are subject to predation. Similarly, parasites can alter host behavior or induce morphological changes, e.g., in coloration, but they usually do not kill their host. Yet, parasitism can compromise the immune system and alter the energy budget of the host.

High population density is a stressor that can affect energy budgets and intraspecific and interspecific competition for space, status or resources. By altering resource availability, changes in growth and size at maturity can be the result. Additionally, these competition-related stressors can affect behavior, for example by limiting the number of suitable mating partners. Also pathogens (e.g., viruses, bacteria and fungi) can lower fitness and fecundity.

It should be realized that the effects of different biotic stressors cannot be strictly separated from each other. For example, pathogens can spread more rapidly when population densities are high, while predation, on the other hand, can limit competition.

Effects of biotic stressors on bioavailability and toxicokinetics

Biotic stressors can alter the bioavailability of chemicals. For example in the aquatic environment, food level may determine the availability of chemicals to filter feeders, as they may adsorb to particulate organic matter, such as algae. As the exposure route (waterborne or via food) can influence the subsequent toxicokinetic processes, this may also change the chemicals’ toxic effects.

Effects of biotic stressors on behavior

Biotic stressors have been reported to cause behavioral effects in organisms that could change the toxic effects of chemicals. These effects include altered feeding rates and reduced activities. The presence of a predator, for example, reduces prey (foraging) activity to avoid being detected by the perceived predator and so decreases chemical uptake via food. On the other hand, the condition of the prey organisms will decrease due to the lower food consumption, which means less energy is available for other physiological processes (see below).

In addition to biotic stressors, also chemicals can disrupt essential behaviors by reduction of olfactory receptor sensitivity, cholinesterase inhibition, alterations in brain neurotransmitter levels, and impaired gonadal or thyroid hormone levels. This could lead to disruptive effects on communication, feeding rates and reproduction. An inability to find mating partners, for example, could then be worsened by a low population density. Furthermore, chemicals can alter predator-prey relationships, which might result in trophic cascades. Strong top-down effects will be observed when a predator or grazer is more sensitive to the contaminant than its prey. Alternatively, bottom-up effects are observed when the susceptibility of a prey species to predation is increased. For example, Cu exposure of fish and crustaceans can decrease their response to olfactory cues, making them unresponsive to predator stress and increasing the risk to be detected and consumed (Van Ginneken et al., 2018). Effects on the competition between species may also occur, when one species is more sensitive than the other. Thus, both chemical and biotic stressors can alter behavior and result in interactive effects that could change the entire ecosystem structure and function (Fleeger et al., 2003).

Physiology

Biotic stressors can cause elevated respiration rates of organisms, in aquatic organisms leading to a higher toxicant uptake through diffusion. On the other hand, they can also decrease respiration. For example, low food levels decrease metabolic activity and thus respiration. Additionally, a reduced metabolic rate could decrease the toxicity of chemicals which are metabolically activated. Also certain chemicals, such as metals, can cause a higher or lower oxygen consumption, which might counteract or reinforce the effects of biotic stressors.

Besides affecting respiration, both biotic and chemical stressors can induce physiological damage to organisms. For instance, predator stress and pesticides cause oxidative stress, leading to synergistic effects on the induction of antioxidant enzymes such as catalase and superoxide dismutase (Janssens and Stoks, 2013). Furthermore, the organism can eliminate or detoxify internal toxicant concentrations, e.g. by transformation via Mixed Function Oxidation enzymes (MFO) or by sequestration, i.e. binding to metallothioneins or storage in inert tissues such as granules. These defensive mechanisms for detoxification and damage control are energetically costly, leading to energy trade-offs. This means less energy can be used for other processes such as growth, locomotion or reproduction. Food availability and lipid reserves can then play an important role, as well-fed organisms that are exposed to toxicants can more easily pay the energy costs than food-deprived organisms.

Interactive effects

The possible interactions, i.e. antagonism, synergism or additivity, between effects of stressors are difficult to predict and can differ depending on the stressor combination, chemical concentration, the endpoint and the species. For Ceriodaphnia dubia, Qin et al. (2011) demonstrated that predator stress influenced the toxic effects of several pesticides differently. While predator cues interacted antagonistically with bifenthrin and thiacloprid, they acted synergistically with fipronil.

It should also be noted that interactive effects in nature might be weaker than when observed in the laboratory as stress levels fluctuate more rapidly or animals can move away from areas with high predator risk or chemical exposure levels. On the other hand, because generally more than two stressors are present in ecosystems, which could interact in an additive or synergistic way as well, they might be even more important in nature. Understanding interactions among multiple stressors is thus essential to estimate the actual impact of chemicals in nature.

References

Fleeger, J.W., Carman, K.R., Nisbet, R.M. (2003). Indirect effects of contaminants in aquatic ecosystems. Science of the Total Environment 317, 207-233.

Janssens, L., Stoks, R. (2013). Synergistic effects between pesticide stress and predator cues: conflicting results from life history and physiology in the damselfly Enallagma cyathigerum. Aquatic Toxicology 132, 92-99.

Qin, G., Presley, S.M., Anderson, T.A., Gao, W., Maul, J.D. (2011). Effects of predator cues on pesticide toxicity: toward an understanding of the mechanism of the interaction. Environmental Toxicology and Chemistry 30, 1926-1934.

Relyea, R.A. (2003). Predator cues and pesticides: a double dose of danger for amphibians. Ecological Applications 13, 1515-1521.

Van Ginneken, M., Blust, R., Bervoets, L. (2018). Combined effects of metal mixtures and predator stress on the freshwater isopod Asellus aquaticus. Aquatic Toxicology 200, 148-157.