Eastern grey squirrels (Sciurus carolinensis) show reduced

antipredator response in high density urban areas

Kwo Mun Wong

Abstract
This study explores the Flight Initiation Distance (FID) of Eastern grey squirrels in response to
varying levels of human exposure in high-density urban and low-density areas. The Optimal
Escape Theory predicts animals to adjust their flight responses based on perceived threat,
balancing costs and benefits. The FID, indicating the distance when an animal starts to escape
from a predator, is influenced by factors such as predator approach speed, directness, and the
type of predator. Habituation, the reduction in antipredator response due to repeated exposure,
and the potential reduction of predation in urban areas are also considered. The study was
conducted in Morningside, Toronto, and involved observing 337 squirrels. Results show a
significantly higher FID in low-density areas compared to high-density urban areas, supporting
expectations based on the Optimal Escape Theory. My findings suggested that human exposure
influences squirrels' antipredator behavior, potentially driven by learning and adaptation to urban
environments, selection as predicted by the optimal escape theory, reduction of predators as a
result of urbanization and a shorter distance to refuge.
Keywords: Flight Initiation Distance, Optimal Escape Theory, Human Exposure, Habituation,
Eastern Grey Squirrels, predation

Introduction
The Optimal escape theory states that animals alter their flight responses according to the level
of threat (Bateman & Fleming, 2014). More specifically, when the risk of predation exceeds the
cost of escape, or in other words, when the cost of remaining in place exceeds the cost of fleeing
(Dill & Houtman, 1989). The fundamental idea is that if the animal escapes too early, it risks
wasting foraging effort, lowering its fitness. If the animal escapes too late, it risks being
captured. Thus, there must be an optimal escape distance that maximizes fitness and is based on
the animal’s ability to balance risks and benefits (Engelhardt & Weladji, 2011). The optimal
flight distance is known as the flight initiation distance (FID) and is defined as the distance at
which the animal starts to escape when approached by a predator (Ydenberg & Dill, 1986). FID
is an indicator of animals’ threat perception and is commonly used to study the Optimal escape
theory (Engelhardt & Weladji, 2011). A huge amount of studies has shown that FID increases
with the risk of predation but decreases with escape cost, including studies on lizards, mammals,
and fishes (Engelhardt & Weladji, 2011).
The assessment of risk is complex and difficult. It encompasses various factors, including
predator approach speed (Cooper, 1997), directness of the approach (Cooper, 1997), distance to
the closest refuge (Dill & Houtman, 1989), starting distance, which is the distance when the
approach starts (Engelhardt & Weladji, 2011), and the type or dangerousness of the predator
(McLean & Godin, 1989). The behavior of the predator also affects the risk; Bateman & Fleming
(2014) showed that unusual behaviors, such as when pedestrians move off their footpath, indicate
higher risk and increase FID. The presence of dogs and vehicles in company with humans, which
is common in an urban setting, can also increase FID (Cooper et al., 2008). A study showed that
predator approach speed and directness interact and influence the flight response (Cooper, 2003).
This adds to the complexity, as it suggests that multiple risk factors might have interactive
effects, making the assessment of the flight response's relationship with risk more difficult
(Cooper, 2003). The escape cost is crucial in understanding the whole picture, but it is not the
focus of this study. It includes the energy spent to forage, the increased chance of injury during
escape, and the loss of social and foraging opportunities (Cooper, 2003).
Other factors, like habituation, might influence the FID (flight initiation distance) of the animal.
It is defined as the reduction in antipredator response when repeatedly exposed to specific stimuli
(Engelhardt & Weladji, 2011). For example, it is well-documented that eastern grey squirrels
show a minimum antipredator response in high urban density areas (Engelhardt & Weladji,
2011). This behavioral plasticity is based on the prey’s ability to learn and distinguish different
levels of threat, adjusting their antipredator behavior accordingly to maximize fitness (Bateman
& Fleming, 2014). Thus, the FID of populations in high vs low density areas can differ
drastically as their past experience and habituation levels are different (Ditchkoff et al., 2006). It
is also important to note that, in general, predation is lower in high-density urban areas compared
to rural or low-density areas, which could reduce the flight response (Engelhardt & Weladji,
2011).
This study investigates the effect of different levels of human exposure on FID using eastern
grey squirrels. It is hypothesized that FID in low density areas will be higher than that in high
density urban areas.

Materials and methods

Eastern Grey Squirrels
Eastern grey squirrels (Sciurus carolinensis) are found in North America, Europe, and Africa and
are one of the most widely distributed tree squirrel species (Bateman & Fleming, 2014). They
appear in two colors: grey or black, with black being the dominant phenotype in Ontario (D.
Smith, 1990). They feed on nuts, acorns, and pecans (D. Smith, 1990). Grey squirrels dig nut
caches and store food underground, which they will dig up in winter (D. Smith, 1990). They
build large leaf nests inside a tree, although they might resort to a leaf nest on top of a large tree
due to the scarcity of suitable tree holes (D. Smith, 1990). Eastern grey squirrels are more active
in the early mornings or in the evening and can reach speeds of 25 km/h, making them very
successful urban adapters (D. Smith, 1990). When alerted, squirrels can produce alarm calls to
warn other squirrels nearby (D. Smith, 1990). Eastern grey squirrels have two breeding seasons,
in January and in June (D. Smith, 1990). Common wild predators of grey squirrels include foxes,
lynx, hawks, and wolves (D. Smith, 1990). In urban areas, cats and dogs are the most common
enemies, while human activities such as driving also kill a large number of squirrels every year
(D. Smith, 1990). Eastern grey squirrels in urban areas can reach high population densities,
ranging from 3 to 10 individuals per hectare up to 51.5 individuals per hectare (Parker & Nilon,
2008). Moreover, they are active all year round, including the time when the study is conducted.
Thus, they are a good model species to study behavioral ecology (Steele & Koprowski, 2004).
Study Sites
The high-density site is in Morningside, bounded by Morningside Avenue, East Morningside
Park, Ellesmere Road, and highway 401 in Toronto Ontario. The neighborhood is entirely
residential with no commercial developments, although it contains unused land intended for
future developments. There are four urban parks in the area I studied. Total population is 11459
(CTs Density Map for the City of Toronto, n.d.).
The low-density site is in Morningside Park below Ellesmere Road. It is a 596-acre park
surrounded by highly urbanized areas (TRCA, 1999). In the 1960s, Highland Creek Park, which
is owned by the city, and the land next to it, owned by the Toronto and Region Conservation
Authority, were combined to create the Morningside Park we have today (TRCA, 1999). There
are two environmentally significant areas in the park, and it has the largest block of forest within
the highland creek watershed and provides habitat for wildlife and rare plant species (TRCA,
1999).
Data collection
Data was collected by students on 6th November for high density areas and 11th November for
low density areas. Observations were made from 8am to 12pm when the squirrels are most
active, searching by foot without tracing steps. When a squirrel is observed foraging, I
immediately approach the squirrel in an aggressive manner, imitating a predator. When the
squirrel started to flee, a marker was dropped on the ground, the flight initiation distance
between the marker and the original position of the squirrel was calculated by multiplying the
number of steps with the length of the shoe.
Statistical analysis
A one-sided unpaired t test was used to test for significant difference between two species.
Unpaired t tests are used as the observations are collected randomly and independently. One-
sided t test is used as we have an expectation, and we are testing if FID is lower in high density
urban areas compared to low density urban areas.

Results
A total of 337 squirrels were observed, 197 from high density areas and 140 from low density
areas. The mean FID for high density areas is 7.36m (SE = 0.27; fig. 1) and 8.41m for low
density areas (SE = 0.4; fig. 1). The mean flighting distance or FID is significantly higher in low
density urban areas compared to high density urban areas (p = 0.0117, t = 2.2278, df = 335; fig.
1)

Discussion
I found that FID is higher in low-density areas than in high-density areas (fig. 1). Other studies
have reported similar results, in which FID decreases with human exposure (Cooper et al., 2008;
Engelhardt & Weladji, 2011; McCleery, 2009). This is expected, as according to the optimal
escape theory, natural selection favors those who can adjust their anti-predator behaviors. This
learning or adaptation would be advantageous as it increases time for foraging and reduces the
energy or cost spent on anti-predator behavior (W. E. Cooper & Frederick, 2007; Stankowich,
2008). McCleery (2009) found that rural Eastern grey squirrels, on average, spent more than
60% of the next 2 minutes after being alerted performing anti-predator behaviors. In high urban
density areas, squirrels did not flee until they were approximately 3m away (McCleery, 2009).
Although the results of McCleery (2009) are more extreme, this proves that human exposure
causes behavior changes in squirrels to maximize fitness, as continuing anti-predator behaviors
in urban areas is a waste of energy. To conclude, Eastern grey squirrels may learn from constant
exposure to humans and reduce antipredator responses towards us. Moreover, humans providing
food might speed up this learning process, making squirrels less alerted by humans (Engelhardt
& Weladji, 2011). However, the optimal escape theory has its limitations; studies have shown
that there is no difference in vigilance behavior in birds between urban and rural areas (Randler,
2003; Ward & Low, 1997). This contradicts the optimal escape theory, as birds in urban areas
should exhibit less vigilance behavior to maximize fitness (Randler, 2003; Ward & Low, 1997).
Although our results could be explained by the optimal escape theory, more research is needed to
confirm its applicability.
Habituation could explain the reduced FID in urban areas under high human exposure. It is the
most common explanation and is defined as the reduction in antipredator response when
repeatedly exposed to specific stimuli (Engelhardt & Weladji, 2011; Labra & Leonard, 1999;
McCleery, 2009). McCleery (2008) found that there were huge differences in FID between
juvenile squirrels and adult squirrels, which supports the reduced response due to habituation, a
learned process. Moreover, Frid & Dill (2001) suggested that antipredator response is innate and
was developed through evolution, so the reduction is more likely due to habituation and not from
individual differences. A similar study on eastern grey squirrels found similar results and
attributed the differences to non-lethal human exposure (Engelhardt & Weladji, 2011). The types
of human activity are important, as non-lethal human activity triggers habituation, but lethal
human activities are found to increase FID (Reimers et al., 2009; Stankowich, 2008).
An alternative explanation for the reduction of FDI in high-density areas is the decrease in
predation overall due to urbanization. Lima & Dill (1990) showed that animals can balance
predation risk and anti-predator activities. This explanation attributes the differences between
high- and low-density areas to a general reduction in predator activities instead of differences in
human exposure. This is supported by Blumstein (2002); they found that species on isolated
islands that are free from predators show a loss of anti-predator behavior. Although some
behavior is innate, evolution has been so rapid that it is lost in a few generations (Blumstein,
2002). Moreover, learned anti-predator behavior will also be lost in the absence of predators
(Blumstein, 2002). However, one study showed that urban fox squirrels did not lose their anti-
predator behaviors towards hawks and dogs; the same level of response is still seen when
humans are paired with these predators (Kittendorf & Dantzer, 2021). Behavior is reduced when
only humans are the stimulus (Kittendorf & Dantzer, 2021). A limited number of studies have
investigated whether squirrels lose their anti-predator behavior in general or just towards
humans, and more research is needed to clarify this problem.
Distance to refuge might influence the results. High-density urban areas might have a shorter
distance to refuge. According to Dill & Houtman (1989), FID increases with the distance to
refuge, as a longer distance represents higher risk. However, numerous studies have critiqued
Dill and Houtman (1989). Engelhardt & Weladji (2011) suggested that their study only tested
distances up to 5m, and many variables such as noise, habitat types, food abundance, and size
could affect the results. Eason et al. (2019) tested the distance to refuge in Eastern grey squirrels
in response to FID and found great variation; they stated that flight trajectory, refuge preference,
and even angles between the human and the tree can affect FID. This shows that the distance to
refuge can only partly explain the differences between high-density and low-density areas.
In conclusion, our study compared FID across high-density and low-density urban areas. The
FID of Eastern grey squirrels is higher with low human exposure and vice versa. The observed
pattern could be attributed to natural selection predicted by the optimal escape theory,
habituation, which reduces squirrels' FID in high-density areas, the reduction of natural predators
in high-density urban environments, and the shorter distance to refuge in high-density areas that
reduces FID. My findings invite future investigations to explore the broader implications of these
dynamics and to gain a better understanding of humans' influence on animals' behavior.
Improvements and future directions
My study only compared high and low-density areas. To gain better understanding, a high-
medium-low human exposure gradient should be used to conduct the study. Aside from FID, I
should measure the flee distance of the squirrel which might be different between high-density
and low-density areas. Since there are so many variables that can affect FID, future studies could
isolate a single variable in the lab and explore its relationship with FID. Additionally, Studies
should focus on investigating whether squirrels lose their antipredator behavior in general or
only towards humans.
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Figures

8.6

8.4
mean squirrel flight distance (m)

8.2

7.8

7.6

7.4

7.2

6.8
High Low
Density

Figure 1. The mean flighting distance of Eastern Grey Squirrel (Sciurus Carolinensis) when
approached by a human in high density and low-density urban areas. The distance between the
approaching human and the initial spot of the squirrel is measured. High density area is in
Morningside, between Morningside Avenue and east highland creek, Toronto, Ontario. Low
density area is in Morningside Park, an urban park in Toronto, Ontario.