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).