Discussion
Our study shows that variation in human activity can profoundly affect
multiple aspects of risk-sensitivity and antipredator responses in
wildlife even over relatively small spatial scales. Specifically, ground
squirrels residing in areas of greater human activity consistently had
shorter FIDs than squirrels residing in adjacent, nearby areas of lower
human activity. Importantly, repeated exposure to human activity also
influenced the post-FID response, as squirrels from high human
disturbance areas also fled shorter distances before stopping to observe
a potential threat following their flight response, and if they fled
into shelter, were consistently faster to emerge from shelter. Squirrels
from high activity sites have likely habituated to high human activity,
thus responding less to an approaching human compared to individuals
that have less experience with humans. While many other studies have
observed animal habituation to non-dangerous humans (Petelle et al.
2013; Vincze et al. 2016; Uchida et al. 2019; Uchida & Blumstein 2021),
it is striking that variation in the degree of habituation emerged over
a small spatial scale (i.e., within a 1-hectare area). Beyond the strong
effects of relative human activity on multiple antipredator behaviors,
we also documented consistent individual differences in the suite of
repeatable behaviors along a general, shy-bold continuum (Wilson et al.
1994) including high among-individual correlations between FID and
post-FID responses for the first time.
Having a highly correlated suite of behaviors may be adaptive or
maladaptive, depending on the situation and environment in which the
animal resides (Trouilloud et al. 2004; Geffroy et al. 2015; Wilson et
al. 2020). In this case, having correlated behaviors throughout the
antipredator response may be beneficial when it comes to predators
(e.g., when real danger is present, animals should both flee readily and
hide for a relatively long time before resuming activity). However, the
correlation may exacerbate unnecessary over-avoidance of humans that can
be a substantial problem in human disturbed environments (Trimmer et al.
2017; Guiden et al. 2019). Unhabituated animals might both flee too
readily from humans (that are not actually dangerous), but also wait too
long to emerge from shelter which may mean a lost opportunity in
foraging time. On the other hand, getting habituated in terms of both
reduced tendency to flee and reduced time spent inactive can be
beneficial. However, if getting bolder (here, when habituating to
humans) carries over to other situations, this can be ecologically
relevant. For example, we know that bolder squirrels pick-up more fleas
(Smith et al. 2021) and have increased venom resistance (Holding et al.
2020). Perhaps most notably, it has been suggested that boldness
associated with habituation to humans can make animals less wary when
encountering actual, dangerous predators, which can obviously be very
costly (Lowry et al. 2012; Geffroy et al. 2015). Thus, anthropogenic
influences on boldness could influence disease transmission and
predator-prey dynamics.
Here, we found that animals that were bolder, apparently due to being
habituated to human activity, were also more readily trapped. Other
studies have found mixed evidence for an association between boldness
and trappability (Biro 2012; Michelangeli et al. 2015; Brehm &
Mortelliti 2018). The observation that trappability predicts
antipredator behavior can have important implications as a systematic
bias when trapping for monitoring, ecological research or pest control
(Biro & Dingemanse 2009; Garvey et al. 2020).
Besides strong effects of human activity and individual differences, the
three main antipredator responses were largely either unaffected or only
weakly affected by the social (presence and number of conspecifics) and
environmental contexts (distance to shelter, vegetation cover) that we
considered. We predicted that animals that are closer to shelter would
exhibit shorter FIDs and that vegetation cover would affect FIDs, but
these factors did not significantly affect FIDs. FIDs were, however,
affected by the social context (group size). In theory, this effect
could have gone either way. If larger groups with “many eyes” (Pulliam
1973) should detect predators sooner, animals in larger groups should
flee sooner (i.e., have larger FIDs). On the other hand, the dilution or
confusion effects (Bertram 1978) can make animals in larger groups safer
in which case, FIDs should be smaller. In fact, FIDs increased with
group size, consistent with the former mechanism. This finding is
particularly interesting given that California ground squirrels are less
vigilant when foraging in groups (Ortiz et al. 2019). Taken together,
this suggests that, on average, individuals foraging in groups may
benefit from both increased energy intake and earlier detection of
threats. However, humans are not a direct threat to this species and
consistently fleeing early due to human disturbance can lead to
decreased energy intake in the long run. Thus, the social information
provided from group foraging may only be beneficial when confronted with
an actual predator.
We also found evidence for more subtle context-dependence in these
antipredator behaviors. In particular, after fleeing (post-FID
response), the decision to ‘stop and look’ versus flee all the way to
shelter was largely environmentally context dependent. Animals showed no
consistent individual differences in this decision. Instead, they were
more likely to flee to shelter if available shelter was closer.
Interestingly, juveniles were generally more likely to flee to shelter
rather than ‘stop and look’; this presumably reflects their greater
vulnerability to predators and, thus, greater fear (Putman et al. 2015).
We believe our findings of high individual-level correlation among
multiple stages of the antipredator response are consistent with our
general conceptual framework, contributing new insights and
opportunities for the study of animal personalities. Future research
should continue to investigate these correlations throughout the overall
antipredator response in other species and the trade-offs animals face
across all stages of prey’s response to risk and not just their initial
flight response. Doing so can also provide more insights on the impacts
of human activity on wildlife behavior, predator-prey dynamics and
ecosystem function.