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.