Introduction
To understand predator impacts on prey and, in particular, non-consumptive effects of predators on prey (Preisser et al. 2005; Peacor et al. 2020), a key issue is to elucidate factors that explain variation in prey responses to perceived predation risk (Lima 1998; Brown & Kotler 2004; Creel & Christianson 2008; Wirsing et al. 2020). The overall prey response is commonly split into two main stages: escape when an attack occurs or appears imminent, and subsequent avoidance often by staying in or near refuge (Lima & Dill 1990; Heithaus et al. 2009). Although this basic framework has long been part of standard predator-prey behavioral ecology, most studies have either quantified escape responses (e.g., flight initiation distances (FIDs); e.g., Stankowich & Blumstein 2005; Moller et al. 2016), or refuge use (e.g., time spent in refuge; Cooper & Sherbrooke 2015). Surprisingly, few have examined both for the same individuals, particularly in the field. Here, we repeatedly quantified the responses of individually marked, free-ranging animals to the approach of a potentially threatening human. We present what we believe is the first study to test for consistent individual differences in multiple stages of the overall prey response to risk: in initial escape tendencies, in behavior during the escape, and in latency to resume activity after spending time in refuge. In particular, our study is, to our knowledge, the first to examine the fundamental point of individual-level correlations among these aspects of the antipredator response. Under field conditions, even with natural variation in context (e.g., distance to refuge, vegetation height, presence of conspecifics), are the same individuals that are more fearful than others in the sense of fleeing more readily also more fearful in the sense of staying longer in refuge before resuming activity? This correlation across stages of the prey response, if it exists, provides an underlying mechanism for a tradeoff involving not just the cost versus benefit of early versus late escape, or early versus late emergence from refuge, but for a tradeoff based on variation in fearfulness expressed across stages. Before describing our field study on ground squirrel antipredator responses, we next provide a bit more detail on the general conceptual overview.
When prey first detect a potential predator, they can, but often do not, immediately initiate an escape attempt. Instead, prey often monitor the predator’s behavior, and only initiate escape when the predator approaches more closely. A standard metric for assessing fear is thus an animal’s flight initiation distance (FID), the distance at which an individual flees from an approaching intruder. Theory predicts that because active escape from predators has costs (e.g., energy and lost opportunities), prey should typically not initiate escape as soon as they detect predators but should instead optimize their FID by fleeing only when predators have come close enough that the costs of not fleeing are higher than the costs of escaping (Ydenberg & Dill 1986). A large literature (e.g., Stankowich & Blumstein 2005; Moller et al. 2016; Morelli et al. 2019) shows that FIDs can depend on characteristics of the predator (e.g., greater FID if predators are perceived to be more dangerous), the prey (e.g., the prey’s state, escape ability, or behavioral type), the social context (e.g., presence of conspecifics), and the ecological context (e.g., availability and distance of refuge). With regard to prey traits, the current interest in animal personalities (Sih et al. 2004a,b; Reale et al. 2007) suggests a need to measure consistent individual differences in FIDs; however, to date, relatively few studies have quantified the repeatability of FIDs in nature (but see Carette et al. 2009; Moller & Tryjanowski 2014; Cabrera et al. 2017).
After animals flee from a predator, they have further decisions to make including whether to run into shelter and if so, when to emerge. Rather than run all the way to shelter, animals sometimes flee and then ‘stop and look’ to apparently re-assess the danger. The distance that they flee before they ‘stop and look’ can be used as an additional measure of fearfulness (i.e., more fearful animals likely have a larger ‘stop and look’ distance). If prey flee to shelter, then a key decision is when to emerge to resume activity (Sih 1992; Cooper & Frederick 2007). More fearful animals likely have a longer latency to resume activity. While FIDs have been measured in many species (Bonenfont & Kramer 1996; Stankowich & Blumstein 2005; Engelhardt & Weladji 2011; Petelle et al. 2013; Moller & Tryjanowski 2014; Uchida et al. 2015), fewer studies have explored post-FID responses (but see Bonenefont & Kramer 1996; Cooper & Sherbrooke 2015; Tätte et al. 2018; Breck et al. 2019) and, to our knowledge, no studies have quantified consistent individual differences (repeatability) of post-FID responses – either in isolation or in relation to other components of the antipredator response.
If FIDs, ‘stop and look’ distances, and latency to resume activity all reflect differences among individuals in underlying fear, then consistent individual differences in these should be positively correlated. These correlations are ecologically important; for example, the core idea that more fearful animals suffer greater opportunity costs (e.g., greater reductions in feeding rate) from avoiding predators hinges not just on them escaping more readily to shelter, but crucially, on them hiding, often for long periods, before resuming activity. It is thus striking that, to our knowledge, no previous studies have tested the hypothesis that larger FIDs are positively correlated with longer latencies to resume activity. Ideally, analyses of multi-stage prey responses to predators should test for effects of both individual differences in behavioral tendencies and multiple aspects of the context (ecological and social) on each stage of the overall response; however, as far as we know, no previous studies have attempted to do that.
We studied the responses of focal animals to approaching humans. With the global expansion of human presence, animal responses to human activity can have important effects on individual and species success (Strasser and Heath 2013; Arroyo et al. 2017). How well animals cope may depend on a variety of factors including their behavior and/or their past experience with human disturbance (Sih et al. 2011, 2012; Lapiedra et al. 2017). In many cases, animals respond to humans as predators, actively avoiding areas of human activity (Oriol-Cotterill et al. 2015; Clinchy et al. 2016; Suraci et al. 2019). In other cases, however, repeated exposure to humans leads to habituation (Stankowich & Blumstein 2005; Geffroy et al. 2015; Blumstein 2016; Uchida & Blumstein 2021). The reduced fear of humans can be associated with a general increase in boldness, exploration or aggressiveness as often seen in animals in urban environments (Moller 2008; Rodriquez-Prieto et al. 2008; Miranda et al. 2013; Uchida et al. 2015; Breck et al. 2019). However, whilst behavioral adjustments in animals inhabiting urban environments are well-documented, less is known about how human activities shape behavior or behavioral variation in animals residing in natural areas, such as reserves or parks that are comparatively insulated from urban disturbance (Gonson et al. 2016; Watson et al. 2016; Corisini et al. 2019).
Here, we examined how variation in rates of human activity shape risk-sensitive behavior throughout multiple steps of the antipredator response in a free-living mammal, the California ground squirrel (Otospermophilus beecheyi ). Ground squirrels are ecosystem engineers, a major prey species in the California grasslands (Smith et al. 2016) and display a suite of behavioral responses to threats (Owings & Ledger 1980; Hanson et al. 1997; Putman et al 2015; Ayon et al. 2017) including human approach (Hammond et al. 2019). While ground squirrels are often deemed pests by humans, they are generally not directly killed by humans. This species therefore offers an interesting opportunity to examine how animals exposed to varying levels of human activity adapt their behavior in the presence of humans. Specifically, we repeatedly recorded both the squirrels’ flight initiation distances (Ydenberg & Dill 1986, Bjorvik et al 2014; Uchida et al. 2015), and their post-FID behaviors as discussed above (Fig. 1). Thus, our study is unique in allowing us to both (1) explore how human activity influences each decision of a squirrel’s antipredator response (i.e., when to flee and whether and how long to shelter) and (2) examine the covariation between different components of the antipredator response. We predicted that human activity would influence multiple components of a squirrel’s risk-sensitivity and anti-predator response. We further predicted that if aspects of the antipredator response are correlated, then an individual’s FID response should also correspond to their risk-sensitivity across other contexts, such as their willingness to enter a trap across multiple potential trapping sessions. Finally, we also examined other factors that might contribute to risk-sensitive decision-making including age and sex of the focal individual, the surrounding microhabitat features, and conspecific presence.