Trade-off 2: The energy acquisition trade-off: Balancing the needs and costs of obtaining energy
To deal with stress, organisms require more energy to fuel metabolism, maintain homeostasis, and mount direct physiological responses to stressors (Romero et al. 2009). Balancing the needs and costs of obtaining energy and, in particular, the costs in terms of predation risk, is a core issue in behavioral ecology, where extensive theory and numerous empirical studies (Sih 1987; Lima 1998; Brown 1999; Houston & McNamara 1999) provide insights that we draw on to understand energy acquisition tradeoffs associated with responding to environmental stressors.
First, and perhaps most basic, is the fact that when physiological stress increases energy demands, the ability to meet those demands depends on food availability. When organisms have regular access to food and, thus, energy, the negative effects of stressors on organismal performance are typically weakened and, in some cases, entirely negated (Hettinger et al. 2013; Mayor et al. 2015; Tosi et al. 2017). Consequently, laboratory experiments that provide organisms with adequate/high food levels might underestimate multiple stressor impacts in nature, where animals are often food-limited (Martin 1995; McCue 2010). In some cases, environmental stressors further exacerbate low food availability if stressor-induced higher energy demands cause consumers to deplete available resources more rapidly, or because the stressors themselves directly lower resource production and availability (Van der Putten et al. 2010; Bruder et al. 2017). When resources are low or there is heightened competition, acquiring energy becomes more energetically demanding.
Importantly, the increased energy demands associated with coping with stressors can require organisms to adopt riskier behaviours (e.g., higher activity, longer foraging bouts, increased time spent in patches with high food but high risk) (Lima 1998; Lienart et al. 2014). For instance, tadpoles have been shown to increase activity and reduce shelter use in response to higher concentrations of a pesticide and lower food availability (Rohr et al. 2004). Although organisms can partially counteract predation risk and buffer possible stressor synergisms by adopting additional vigilance, or social foraging strategies (Killen et al. 2016), ultimately, under natural conditions, the need to cope with stressors physiologically might often entail exposure to increased predation risk. Alternatively, because animals often respond to high predation risk by exhibiting antipredator behaviours that reduce energy intake this can constrain the ability of organisms to build and maintain the capacity to cope with stressors physiologically.
In the context of the classic risk-reward foraging tradeoff, a key under-studied topic is the spatial or temporal correlations among stressors, food levels and predation risk. Even if stressors are uncorrelated with food and predation risk, as noted above, the need to acquire more energy to cope with stressors physiologically can require increased exposure to predation risk. Thus, stressor exposure and predation risk can become indirectly correlated through the organism’s behavior (see analogous phenomenon concerning behaviorally mediated stressor ‘co-occurrence’ in Box 4, Figure 4). If, instead, stressors are negatively correlated with predation risk (e.g., if avoiding stressors in space or time causes organisms to be more active in places or times when predation risk is particularly high), the cost of multiple stressors can be greatly amplified. To date, few studies have quantified these spatiotemporal correlations and how organisms might balance them adaptively (or not). Predation risk alone can induce physiological stress responses in prey (including elevated stress hormones and metabolic rate) and altered stoichiometry (Rinehart & Hawlena 2020). Although a meta-analysis found that the presence of a second stressor (most commonly food limitation or elevated temperature) did not generally influence prey stoichiometry beyond effects of predation risk, this result comes from relatively few studies that varied considerably in observed effects (Rinehart & Hawlena 2020).
In some cases, stressors interfere with an organism’s sensory system and ability to avoid predators, leading to a synergistic negative effect of the stressor and background predation risk (Reeves et al. 2010; Hayden et al. 2015; Polo-Cavia et al. 2016; Martinet al. 2017; Sievers et al. 2018). For example, metal and pesticide contaminants indirectly increase mortality in frogs, because these contaminants can compromise predator recognition systems and avoidance behaviours, leading to higher predator attack rates and inflicted injuries (Reeves et al. 2010; Hayden et al.2015). Similarly, fluoxetine exposure in mosquitofish, Gambusia holbrooki , inhibits neurotransmission pathways, leading to relaxed anti-predator behaviour and maladaptive responses to high predation risk (Martin et al. 2017).
If physiological stressors, foraging activity, and predation risk pose conflicting demands, the costs of stressors can then involve a mix of direct costs, where the stressors themselves cause harm (e.g., allostatic overload resulting in reduced fitness), and indirect costs (e.g., exacerbated hunger, higher predation risk) associated with the need to get energy to fuel physiological responses. When might we expect direct versus indirect costs to be larger? Parallel theory on balancing risks and foraging offers intuitive, qualitative predictions (Brown 1999; Houston & McNamara 1999). When food availability is high and predation risk is low, animals need not be very active to obtain sufficient energy to fuel physiological responses to stressors. As a result, the stressors’ direct costs and their indirect fitness costs, in terms of predation risk, should be of similar, relatively small magnitude, so long as direct effects are mitigated via abundant energy (Hettinger et al. 2013; Mayor et al. 2015). In contrast, with low food levels, the activity needed to acquire sufficient energy to fuel physiological responses to stressors can require exposure to higher predation risk. The main cost of the stressors might then be increased predation risk and not mortality from the stressors per se. Notably, this indirect cost is not addressed in standard laboratory experiments, where focal organisms are not exposed to actual predation. On the other hand, if the relationship between activity and predation risk accelerates (e.g., if foraging activity above a threshold level causes a pronounced increase in predation risk), then this can constrain activity (and energy intake) to be relatively low for safety, and, thus, constrain investment in physiological responses, resulting in greater direct costs of stressors. These intuitive qualitative predictions should be rigorously explored with quantitative models and empirical experiments to address stressor-foraging-risk trade-offs.