Toward the emergence of a new coping style in predator free-areas
The presence of predators is a key driver that influences the structure of behavioral syndromes (Réale & Festa-Bianchet 2003; Smith & Blumstein 2012). Thus, by extirpating predators, or protecting prey from predation risk, correlations between personality traits may become decoupled (Bell 2005; Bell and Sih, 2007) with a series of cascading effects on the underlying physiology. The sudden elimination of predators following some HIRECs could render behavioral and physiological traits associated with antipredator responses as “useless”. Indeed, natural selection favors antipredator phenotypes that efficiently reduces predation risk. But when the risk is low, these costly phenotypes, including vigilance, high HPI/A activity, or flying capacities, may become counterproductive. Consequently, constraints on these phenotypes are released and the correlation between traits is lost (Fig. 2).
Nevertheless, these effects observed in response to the reduction of predation seem to come with additional constraints related to the presence of human and their associated activities. Indeed, in response to the presence of human, there might be selection for some specific traits leading to new correlation between traits (Fig. 2). However, the direction, intensity and speed of this selection are still unclear, and we therefore face difficulties in predicting animals’ responses to human presence.
Response to domestication can be used as a guide to predict the fate of individuals in predator free areas and in interactions with human. Most of our knowledge on the subject comes from foxes (Vulpes vulpes ) that have been domesticated for now more than 40 generations (Trut 1999), with mixed results. Selection for tameness led to a decrease in fear-related traits (Trut 1999), cortisol production and associated gene pathways (Trut et al. 2009) which means that animals are now more bold and proactive (Fig. 1.3.1.3). However, it also decreased aggressiveness (Trut 1999) and increased social cognitive abilities (Hare et al. 2005) and neurogenesis (Huang et al. 2015), which is consistent with them being more reactive (Rauw et al.2017) (Fig. 1.3.1.3). Notably, however, is that brain size reduction, which often correlates with behavioral flexibility (Sol et al.2005, 2008), characterizes domestication in most species (excluding foxes and mice) (Wilkins et al. 2014), and this, associated with the development of routine-like behavior linked to a closed environment (Rauw et al. 2017), would suggest that we should expect reduced cognitive skills.
In the case of urbanization (Fig. 1.3.1.2), human contact also leads to increased boldness (Shochat et al. 2006; Coleman et al.2008; Møller 2012; Thompson et al. 2018), and a reduced HPI/A responses (Atwell et al. 2012), which should tend to create more proactive individuals. Nevertheless, urbanization also comes with increased cognitive abilities (Audet et al. 2015), and behavioral plasticity (Carrete & Tella 2011; Sol et al. 2013; Thompsonet al. 2018), characteristics of reactive individuals. In the context of urbanization, it is however important to notice the difficulty to determine whether these characteristics emerged from differential colonization according to an individual’s traits, or from an evolutionary response that selected for specific traits. In other words, did bold individuals invade towns (Fig. 1.3.1.2, dashed purple arrow), or did shy individuals evolve towards boldness in urbanized areas (Fig. 1.3.1.2, solid grey arrow) (Sol et al. 2013)?
In the context of tourism and ecotourism, similar results to those seen with urbanization and domestication have been observed in animals that are in frequent contact with humans. We have seen that boldness has increased (Geffroy et al. 2015b; Arroyo et al. 2017), as has neurogenesis (Geffroy et al. 2018). However, baseline and post stress cortisol responses seem to strongly depend on the intensity with which humans interact with animals, with severe disturbance generally increasing cortisol production (Geffroy et al. 2017) (Fig. 1.3.1.1).
Overall, wild animals exposed to HIREC that relaxes selection on antipredator behavior and increases human contact would likely be bolder but also less aggressive, more plastic in their response, with higher cognitive abilities and lower HPI/A responses. We suggest a new term — “preactive”— in that individuals are part proactive and part reactive. The emergence of this new coping style would be the result of uncoupling initatially associated traits (Fig. 2A), by a first step of relaxed selection due to the creation of a human-shield (Fig. 2B) and a second step where animals associated with humans selectively learn (and/or have evolved) to deal with this new situation by displaying overall decreased aggression, increased boldness and decreased HPI/A reactivity while improving their capacities to be plastic in association with higher neurogenesis (Fig. 2C).