Flush early and avoid the rush: a general rule of antipredator behavior?

Well-understood subjects should lead to the development of general hypotheses, rules, and ultimately, laws. Unlike the fields of physics, which has many laws (e.g., gravity, thermodynamics, etc.), ecology, which has a series of biogeographic rules (e.g., Allen’s, Bergmann’s, Cope’s, Gloger’s, Rapoport’s rules), and evolution, which has a grand theory (evolution by natural selection), behavioral ecology lacks such generalizations. There is a great deal of controversy about whether fields other than physics can or should have laws, and this has led to a spirited debate in the ecological literature (e.g., Lawton 1999; Mitchell 2000; Murray 2000; Jørgensen 2002; Colyvan and Ginzburg 2003; Lange 2005). I would like to acknowledge this controversy but note (that with some exceptions) behavioral ecologists often focus on documenting and understanding behavioral variation rather than summarizing it into formal hypotheses or rules. Some notable exceptions may include Hamilton’s rule (Hamilton 1964a, 1964b) and Trivers’ various hypotheses (Trivers 1971, 1974; Trivers and Willard 1973). I also acknowledge that some may consider these too restrictive and not having the precise predictive ability of what we would want a generalization to contain. Indeed, one might argue that a lesson from behavioral ecology is that all individuals face trade-offs, but this itself does not allow us to predict behavior in the way that a formal rule would. Rules, however specific, allow us to predict behavior. In this forumpiece, I would like to propose a hypothesis that, with time, may rise to a rule. The hypothesis is that ‘‘animals will flee approaching predators soon after they detect and identify them as a threat to reduce or minimize ongoing attentional costs of monitoring the approaching predators. ’’ The implication of this ‘‘flush early and avoid the rush hypothesis’’ is that species that first detect threats at a greater distance (e.g., because of body size, eye size, habitat visibility, etc.) will be more distracted by approaching threats than those who are unable to detect them until they are closer. This differential distraction has implications for coexistence with both predators and humans. I pose this hypothesis in the spirit that by trying to make broad generalizations, and testing them, the field of behavioral ecology will advance well beyond the great conceptual advances made in the 1970s and 1980s (Birkhead and Monaghan 2010). Advances will range from identifying the conditions (i.e., state space, species, etc.) under which broad generalizations are possible, to perhaps generating truly universal rules. Animals may perceive humans as predators (Frid and Dill 2002), and this simple observation has allowed the systematic study of antipredator behavior across many taxa. When a human walks toward an animal, species that use flight to escape their predators will inevitably move away. This response is called ‘‘flight initiation distance’’ or, in the wildlife management literature, ‘‘flush distance’’ (Stankowich and Blumstein 2005). In many cases, prior to flight, the prey will orient or otherwise look at the approaching threat. This response is called ‘‘alert distance’’ (Blumstein et al. 2005). The distance from which a human begins approaching an individual is called ‘‘starting distance’’ (Blumstein 2003). In many cases, starting distance is used as a proxy for alert distance because it is often difficult to accurately identify when an animal becomes alert to an approaching threat. Indeed in some cases, animals may flush as soon as they become aware of an approaching threat (e.g., Stankowich and Coss 2006). The field will advance as we apply more sensitive assays to identify detection (e.g., cardiac or other ‘‘cryptic’’ autonomic nervous system responses—Blumstein and Bouskila 1996), so that we can better study the decision to flee. Flight initiation distance has been extensively reviewed (Stankowich and Blumstein 2005) and modeled (Ydenberg and Dill 1986; Blumstein 2003; Cooper and Frederick 2007). Studying factors that influence both flight initiation distance and alert distance has led to both theoretical and applied insights. Although animals may dynamically modify their alert and flight initiation distances to manage their response to threats, there is a species-specific component to these antipredator responses as well (Blumstein et al. 2003), and it is possible to study the evolution of both alert distance and flight initiation distance (Blumstein et al. 2005; Blumstein 2006). A general observation that emerges from studies of birds, mammals, and some lizards is that there is a statistical relationship between the distance the human starts walking toward the animal and both the alert distance and the flight initiation distance (Blumstein 2003; Blumstein et al. 2005; Cooper 2005; Stankowich and Coss 2006; Cooper et al. 2009) and that there is a statistical relationship between the alert distance and the flight initiation distance (Cárdenas et al. 2005). The relationship between starting distance and flight initiation distance is not always present (Cooper 2005), may in some circumstances be an artifact (Cooper 2008), and may be modified by other risk factors (Cooper et al. 2009), but it is nevertheless very common. The relationship between alert distance (which can’t always be properly measured, and thus starting distance is sometimes used as a proxy) and flight initiation distance seems more robust. Indeed this observation extends beyond vertebrates. While recently studying a terrestrial hermit crab (Coenobita clypeatus), I noticed that the distance a hermit crab first responded to an approaching human was highly correlated with the distance at which it withdrew into its shell and hid (r = 0.916, P , 0.0001, n = 60). This hiding initiation distance (Chan et al. 2010) is an analog to flight initiation distance in a species that hides, rather than flees, from approaching humans. This general relationship—seen in birds, mammals, lizards, and now an invertebrate—is not simply driven by the fact that animals that are first approached at a very close distance must orient and flush at a closer distance than those who are first approached at a farther distance. Indeed, the range of starting distances in well-studied species is broad (Blumstein et al. 2005). And, even if one starts approaching an animal from a relatively close distance, they often fail to respond for a while. If anything, there may be a bias in the other direction in that