A common behavioral trend observed in urban animals is that they tend to be bolder compared to their rural counterparts. This behavioral shift can enable urban animals to deal with the unique stressors of urban life and may set the stage for urban adaptation. A common way to quantify boldness is to measure flight-initiation distance, or FID: the distance at which an animal flees from an approaching potential predator (typically a human). And although previous studies have shown that urban animals from diverse taxa exhibit this response (check out: Skirting Skinks: Are Lizards Learning to Live Among Humans? and No city for shy dog: Urban coyote are bold and explore more), the relative contributions of decreased vigilance versus increased habituation are not always clear. Even within a species, some traits related to boldness appear to be innate while others are more influenced by environmental conditions (we talked about this in Urban Dragons are Innately Bold). A recent paper by Kenta Uchida and colleagues in Behavioral Ecology attempts to clear up what exactly FID studies tell us about boldness and provides a novel framework to disentangle these factors, which they test in Eurasian Red Squirrels (Sciurus vulgaris).
Lazy or fearless? Either way = shorter FID
The problem with many urban FID studies is that animals may have altered escape responses to humans because of either decreased vigilance or increased habituation. This may seem like splitting hairs, but these two phenomena represent very different types of responses. Vigilance is a response to a general threat. In urban habitats the predator communities are often altered and predation threats reduced. For some species this means they can afford to be lazy when it comes to watching out for potential predators. Habituation, on the other hand, is a risk assessment response to a specific threat. With increased habituation, urban animals have learned through repeated exposure that specific potential threats (e.g., humans) pose no real danger. In both cases, the fear response is dampened and the conclusion that the animals are more “bold” may be drawn.
What’s the problem with this? Well to start, these responses have unique implications for urban persistence of a species and of their adaptive potential in urban environments. A species that exhibits increased habituation may still be able to distinguish different types of threats and respond appropriately, whereas a species that exhibits generally decreased vigilance may be susceptible to predation by non-human predators. Increased boldness in urban animals may be attributable to either, or both, of these processes.
Teasing apart vigilance from habituation
The authors propose a way forward for future studies. They suggest that vigilance is best measured by alert distance (“AD”, the distance at which an animal first notices the approaching threat), whereas flight-initiation distance better estimates risk-taking behavior and habituation. They combined these two metrics with exposure to different types of threats: humans, a stuffed red fox, and a novel object (stuffed red fox covered in a black plastic bag), and tested their framework on Eurasian Red Squirrels in Obihiro city in the Tokachi region of Hokkaido, Japan. They sampled squirrels from six urban parks and four forest sites in the region.
Consistent with previous work by Uchida (e.g., shorter FID and seasonal fluctuations in urban squirrels), the authors found that urban squirrels had both shorter alert distance and flight-initiation distance compared to non-urban squirrels. Rural squirrels fled at twice the distance as those from the city! Interestingly, alert distance did not vary with different types of approaching threats but FID did — but only in the urban animals! Urban animals allowed humans to get much closer before fleeing compared to their response to a stuffed fox. Rural squirrels, on the other hand, fled readily regardless of the threat type.
Uchida and coauthors extend their framework to draw more general conclusions about vigilance and habituation in other taxa. Vigilance can be represented by AD, but habituation they argue is better represented by the difference between AD and FID. This “Relative Tolerance”, or “RT”, represents the buffer zone in which the animal recognizes a human as a potential threat but has not yet decided to respond. When applied to their squirrel data, they found that urban squirrels had a 21% reduction in AD and a 31% reduction in RT compared to rural squirrels and conclude that habituation is relatively more important than reduction in vigilance in determining bold urban behavior in this species.
Bold as a… squirrel?
These findings of Uchida and colleagues are significant because they suggest that urban squirrels are bolder because of both reduced vigilance and habituation. The finding that AD was reduced in urban animals regardless of the threat type supports the hypothesis that urban squirrels are generally less vigilant compared to rural squirrels. The finding that FID was reduced in urban animals differentially in response to the three threat types suggests that urban animals are still able to accurately assess risk and respond appropriately. That they allowed humans, of all the threats, to approach most closely, supports a hypothesis of increased habituation.
Understanding relative contributions of vigilance and habituation to urban behavioral shifts is important from a conservation perspective. If increased boldness is due mainly to decreased vigilance and not to increased habituation, then bold urban animals may actually be more susceptible to predation by novel domestic predators like cats. However, if increased boldness also involves a shift in habituation reflecting appropriate risk assessment and eliciting appropriate flight responses, then such a behavioral shift is likely to be adaptive in urban habitats. The combination of increased habituation with accurate risk assessment may be a key behavioral trait enabling urban success in Eurasian Red Squirrels and other species worldwide. It is in these species that we are most likely to also observe adaptive shifts in other phenotypes as they are exposed to novel stressors in the more drastically altered portions of urban environments.
Featured image from Wikimedia Commons: Ray eye, Eichhörnchen Düsseldorf Hofgarten edit, CC BY-SA 2.0 DE
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