Landscape of human fear in Neotropical rainforest mammals

Abstract

The landscape of fear has profound effects on the species behavior, with most organisms engaging in risk avoidance behaviors in areas perceived as riskier. Most risk avoidance behaviors, such as temporal avoidance, have severe trade-offs between foraging efficiency and risk reduction. Human activities are able to affect the species landscape of fear, by increasing mortality of individuals (i.e. hunting, roadkill) and by disruption of the clues used by the species to estimate predation risk (e.g. light pollution). In this study, we used an extensive camera-trapping and night-time light satellite imagery to evaluate whether human activities affect the diel activity patterns of 17 species of rainforest dwelling mammals. We found evidence of diel activity shifts in eight of 17 analyzed species, in which five species become 21.6 % more nocturnal and three species become 11.7% more diurnal in high disturbed areas. This activity shifts were observed for both diurnal and nocturnal species. Persecuted species (game and predators) were more susceptible to present activity shifts. Since changes in foraging activity may affect species fitness, the behavior of humans’ avoidance may be another driver of the Anthropocene defaunation.

Introduction

The biosphere is becoming increasingly modified by human activities, where 75% of the world area experiences measurable amounts human pressure (Venter et al., 2016). Activities such as the direct removal of natural forests and grasslands to allocate croplands, livestock pastures, urban development and expansion of road networks are the main drivers of the reduction of the natural biomes (Mittermeier et al., 2004). As a consequence, the populations of innumerous species have been also severely impacted by direct and indirect human driven habitat modification and harvesting, with 25 % of mammals, 13 % of birds and 41 % of amphibian species being considered threatened to some degree (IUCN, 2018). Moreover, beyond the direct habitat destruction and species overharvesting, the effects of human activities have also discreet but equally pervasive consequences on population dynamics, caused by changes in the species perception of an area as safe or dangerous (Frid and Dill, 2002).

All species on Earth evolved strategies to avoid predation and are capable of modulate their behavior to achieve the energetic daily demands while avoiding being killed. The oldfield mice (Peromyscus polionotus), for instance, reduces predation risk by foraging on safer areas, under vegetation shelter and during darker nights, while avoiding open areas especially under the moonlight (Orrock et al., 2004). In a similar way, the paca (Cuniculus paca) and nine-banded armadillo (Dasypus novemcinctus), also avoid foraging under the bright full moon, when the perceived predation risk is higher, but concentrate the foraging on new moon nights, when the perceived risk is lower (Harmsen et al., 2011).

The spatial and temporal variation in risk perception by the species is called the “landscape of fear”, and have profound effect on the species ecological interactions along both space and time (Laundre et al., 2010). The landscape of fear perceived by elks in response to reintroduced wolves, is directly related with the herbivory levels along the Yosemite National Park, with higher herbivory levels occurring on areas perceived as safer (Laundre et al., 2010). The landscape of fear perceived by a predator species also affects the distribution of its preys, with higher prey density on areas perceived as risky by the predator (Muhly et al., 2011). Fear have strong effects in foraging efficiency (Verdolin, 2006), and the species’ choice about how much risk is acceptable depends on the cost-benefit ratio of forage in dangerous areas and on the amount of information available to estimate the risk (Bouskila and Blumstein, 2002).

It is important to highlight that the landscape of fear is not based on the real predation risk, but in the individuals’ perceived predation risk. Foraging individuals rarely have complete knowledge about the real predation risk they are exposed, and therefore, they usually estimate the risk based on environmental clues, such as light intensity, canopy density, and noise (Orrock et al., 2004; Verdolin, 2006). This happens because it is safer to estimate the risk by indirect methods than rely on directs detection of a predator nearby, when it may be too late. It is also less harmful to overestimate the predation risk and lose some foraging efficiency, than to underestimate the risk, which can lead to death by predation (Bouskila and Blumstein, 2002; Frid and Dill, 2002). These non-lethal interactions between prey-predator can have even bigger effects on ecosystems dynamics than direct prey-predator interactions (Preisser et al., 2015).

Since the wildlife estimate the predation risk mostly based on clues, human activities can easily confound these clues and lead to false risk estimations, causing entire populations to live and behave under a level of risk perception which is disconnected with the reality, creating landscapes of fear that did not correspond to the real distribution of risks (Frid and Dill, 2002). Wildlife can perceive the noise of vehicles, agriculture machinery, airplanes, electric illumination and even the simple presence of humans as predation risk (Frid and Dill, 2002). As consequence, the high risk perception is known to increase stress hormones (Zbyryt et al., 2018), reduce feeding efficiency (Orrock et al., 2004) and reproductive success (Sheriff et al., 2009). In addition, it can also trigger risk avoidance behaviors, such as the spatial and temporal avoidance.

Temporal avoidance between the predator and prey is the risk avoidance behaviors in which the prey shift its normal diel activity period to become active on a safer period, thus, reducing the chances of encounter a predator or any other threat (Saleni et al., 2007). It is also an alternative and/or complement for spatial avoidance (i.e. avoid risky areas) when the latter is not possible due to low habitat availability, or not enough to avoid conflicts (Martin et al., 2010; Saleni et al., 2007). However, since most species are not cathemeral (i.e. adapted to be equally active at any period of the day), shifts in diel activity period can negatively impact the species capability to locomote in the environment, find food, detect mates and predators (Bennie et al., 2014; Gaston et al., 2014). Despite its drawbacks, temporal avoidance has been showed as a common strategy used by mammals under human disturbed areas (Gaynor et al., 2018).

Since camera-trap data is widely used in research and conservation efforts, but human-driven disturbances not always produce detectable changes in the frequency of species records, we used camera-trap data to test for evidences of temporal avoidance behavior of forest-dwelling mammals in response to human-driven disturbances. We expected to: 1) observe temporal shifts on poached or persecuted species, such as ungulates, armadillos and wild felids (Bitetti et al., 2008; Cullen et al., 2000; Espinosa and Salvador, 2017; Gaynor et al., 2018); 2) confirm temporal shifts to occur mainly towards nocturnality, with species becoming relatively more nocturnal in more disturbed areas (Gaynor et al., 2018); 3) confirm no temporal avoidance in response to human disturbance by small body sized non-poached species, such as opossums (Didelphis spp.) small rodents, species that increase density in fragmented landscapes, such as squirrels (Koprowski, 2005; Mendes et al., 2016), and synanthropes (i.e. which benefit from association with humans), such as dogs (Paschoal et al., 2012).