Box 4. Animal behavior can redefine ‘multiple stressors’
The concept of ‘multiple stressors’ traditionally deals with stressors
that co-occur in time and space, and, thus, the affected organism is
exposed to these stressors simultaneously. However, multiple stressors
need not co-occur in time or space or affect a focal organism
simultaneously to have interactive, potentially synergistic effects that
determine the organism’s survival and fitness. A prime driver of such
unexpected potential stressor interactions is animal behavior. By moving
across natural landscapes that can exhibit extensive heterogeneity in
the spatial distributions of stressors (e.g., involving variation in
elevation, moisture, salinity, turbidity, pollution, natural and foreign
predators), animals can determine the suite, relative exposure,
sequence, and spatiotemporal overlap of stressors they will face. Thus,
stressors separated in time or space or both (Fig. 5) can interact with
one another indirectly at the organismal level, akin to analogous
indirect interactions, such as apparent competition (Holt 1977) and
apparent mutualism (Abrams et al. 1998; Rudolf 2008). Interactive
effects of multiple stressors that do not co-occur over space and/or
time expand the concept of multiple stressors and are candidate drivers
of population declines in natural systems (Fig. 5).
For non-co-occurring stressors to interact at the organismal level
requires that at least one stressor involved imposes at least one
carryover effect: a physiological and/or behavioral effect of a
stressor(s) that lingers after direct exposure ceases, allowing this
stressor’s effect to interact with effects of future stressors.
Carryover effects on physiological stressor responses have been observed
in many systems; for example, bivalves have decreased immune response
following temperature stress, which makes them more susceptible to
disease-based stressors (Rahman et al. 2019). Damselfly larvae
previously exposed to food limitation and heat waves suffered
considerably lower growth rates and higher mortality when later exposed
to an agricultural pesticide (Dinh et al. 2016). Behavioral
carryover effects have also been observed: e.g., tadpoles from high-risk
environments are generally more active, which increased survival in
response to pursuit predators in the future (Ferrari et al.2015).
Carryover effects may be particularly pronounced for stressors
experienced during development. Experience with a stressor can lead to
acclimation via phenotypic (either physiological or behavioral)
plasticity such that the effect of experience with that stressor in the
future is altered. Indeed, such developmental experience can lead to
permanent changes in behaviour or physiology, resulting in improved
performance in the presence of the stressor(s) later in life (Schnurret al. 2014). For example, the keystone sea hare species,Stylochelius striatus, significantly reduced its locomotion speed
and rate of correct foraging decisions following exposure to elevated
temperature and p CO2. While exposure to these
stressors during development still resulted in decreased performance in
adults, developmental exposure lessened the severity of the impacts,
suggesting beneficial phenotypic plasticity (Horwitz et al.2020).
The carryover effects of developmental exposure to a single stressor on
responses to different, future stressors is less well understood despite
the potentially impactful changes to organisms as a result of
acclimation. For instance, warm-acclimated common minnows
(Phoxinus phoxinus ) had larger brains compared to cool-acclimated
fish but made more errors in exploring a maze, suggesting that
maintaining physiological function under stress can result in cognitive
impairments (Zavorka et al. 2020). Developmental stress has been
shown to affect a variety of behaviors including foraging (Crinoet al. 2014; Chaby et al. 2015), learning (Brust et
al. 2014; Kriengwatana et al. 2015), social network position
(Boogert et al. 2014) and the development of behavioral syndromes
(Edenbrow & Croft 2013; Hope et al. 2020) that may interact with
the ability to respond to future challenges.
Though far less studied, carryover effects can also manifest over much
shorter timescales, with the sequence and relative magnitude of stressor
exposure determined not by temporal variation in the stressors
themselves, but instead by temporal variation in spatial patch use by
the focal animal. By simply moving through its home range or migrating
between distant locations, an animal can be affected by spatially or
temporally separate stressors at sufficiently close points in time for
interactions to manifest. For example, rainbow trout (Oncorhynchus
mykiss ) use shelters to avoid predators, however, when they compete for
shelters they are at an increased risk of contracting trematode
parasites from outside habitat patches (Mikheev et al. 2020).