ANIMAL BEHAVIOUR, 2007, 74, 153e158
doi:10.1016/j.anbehav.2006.11.019
Vigilance during food handling in grey squirrels,
Sciurus carolinensis
I. J OAN NA MA KOWS KA & DON A LD L. KRA MER
Department of Biology, McGill University
(Received 19 July 2006; initial acceptance 6 September 2006;
final acceptance 29 November 2006; published online 20 June 2007; MS. number: A10516)
Foraging and vigilance conflict in animals that lower their head during food search and handling, but it is
less clear whether these activities conflict in animals that handle food with the head raised. In these species, at least part of the foraging process is physically compatible with vigilance. Nevertheless, both vigilance and food handling require cognitive resources, so animals may not be vigilant whenever their
head is raised. We tested whether grey squirrels are vigilant when they are handling food items held in
their forepaws while in a semiupright posture. If vigilance occurs during handling, we predicted that squirrels finding food in a location with a partially blocked view would change location before handling to
improve visibility. Because this test assumes that the benefit of vigilance during handling is greater than
the cost of moving, we tested small food items (sunflower seeds) in which the temporal cost of changing
position on the rate of food intake was relatively high and large items (crackers with peanut butter) in
which the cost of changing position was relatively low. When handling crackers, squirrels that had their
lateral view obstructed at the food presentation site changed to a position with a better view more often
than controls or squirrels that had their overhead view obstructed. When handling sunflower seeds, squirrels never changed their position. These results support the view that squirrels are vigilant during semiupright handling, but that vigilance may be sacrificed if it leads to high foraging costs.
Ó 2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Keywords: antipredator defence; foraging; grey squirrel; perception; Sciuridae; Sciurus carolinensis; vigilance; vision
Theoretical models of vigilance usually assume that
foraging animals have their heads down and cannot
detect predators, while vigilant animals have their heads
up and cannot forage (Pulliam 1973; Pulliam et al. 1982;
Lima 1987; McNamara & Houston 1992). Empirical studies sometimes follow this assumption by categorizing animals with their heads up as ‘vigilant’ and those with
their heads down as ‘nonvigilant’ (e.g. Jones 1998; Cowlishaw et al. 2004). Lima & Bednekoff (1999) challenged
this dichotomy by showing that foraging birds can detect
predators when their head is down, although detection
ability is reduced in this position. One may also question
whether animals are vigilant whenever their heads are
raised. Foraging animals may raise their heads for several
Correspondence and present address: D. L. Kramer, Department of
Biology, McGill University, 1205 Avenue Docteur Penfield, Montreal,
Quebec H3A 1B1, Canada (email: [email protected]).
I. Joanna Makowska is now at the Animal Welfare Program, Faculty
of Land and Food Systems, University of British Columbia, 2357
Main Mall, Vancouver, BC V6T 1Z4, Canada.
0003e 3472/07/$30.00/0
reasons. These include handling (e.g. birds: Lima 1988;
Popp 1988; rodents: Bakken 1959; ungulates: Underwood
1982; primates: Treves 2000), searching for the next food
item (e.g. ungulates: Spalinger & Hobbs 1992; Fortin
et al. 2004a; primates: Cowlishaw et al. 2004), moving
away from competitors or towards another patch (e.g. ungulates: Fortin et al. 2004a) and monitoring conspecifics
(e.g. birds: Coolen & Giraldeau 2003; primates: Treves
2000). Because they require attention, these foraging
activities are not necessarily any more compatible with
predator detection than are search and pursuit of food
items with the head down. For example, blue tits, Cyanistes caeruleus, that were handling difficult prey were
not more likely to detect a predator when their head was
raised than when their head was lowered (Kaby & Lind
2003). Several authors have recognized that predator detection may be limited during handling if the animal is
simultaneously searching for the next item or patch (Illius
& FitzGibbon 1994; Cowlishaw et al. 2004; Fortin et al.
2004b). These and other authors have assumed, however,
that handling that does not demand visual attention
153
Ó 2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
154
ANIMAL BEHAVIOUR, 74, 1
(e.g. chewing or using the mouth to remove inedible
components) would not affect vigilance (Lima et al.
1985; Illius & FitzGibbon 1994; Cowlishaw et al. 2004;
Fortin et al. 2004b). This is not necessarily the case, because simultaneous performance of multiple tasks can
result in interference between them (Shapiro 2001;
Luck & Vecera 2002; Marois & Ivanoff 2005; Tombu &
Jolicoeur 2005).
Evidence for vigilance during handling is limited. Popp
(1988) reported that American goldfinches, Carduelis tristis, decreased scan rate and increased scan duration
when eating sunflower as compared to niger seeds, apparently because they were able to scan while handling the
sunflower seeds. Lima (1988) showed that dark-eyed juncos, Junco hymenalis, increased their preference for food
items that required longer head-raised handling as flock
size decreased. Because vigilance often increases as group
size decreases, Lima inferred that the preference was
related to the need for increased vigilance. Lima et al.
(1999) also found that juncos, provided with superabundant food to eliminate competition, increased their
head-up seed-husking times when in smaller groups and
further from cover, also implying that vigilance is
obtained during handling. Cresswell et al. (2003) reported
that chaffinches, Fringilla coelebs, that fed at a higher rate
also raised their heads at a higher rate and had a shorter
response latency to a model predator, suggesting that
a higher rate of handling increased vigilance. However, response latency did not increase with the proportion of
time that the head was raised, which the authors argued
was related to a lower probability of detection as the duration of the vigilance bout increased. Cowlishaw et al.
(2004) showed that when samango monkeys, Cercopithecus mitis erythrarchus, fed on foods for which the handling
time did not require visual attention and was long relative
to the time required to search for the next food item, the
slope of the negative relationship between foraging rate
and vigilance was reduced. This result suggested that
some handling time was devoted both to vigilance and
to finding the next food item. Fortin et al. (2004b) observed apparent scanning behaviour by elk, Cervus canadensis, while the elk gradually chewed and swallowed
clumps of vegetation held in their jaws, although the
authors also noted occasions when chewing stopped during apparent heightened vigilance, indicating potential
incompatibility between such handling and vigilance.
An alternative approach to determining whether vigilance occurs during handling is to test whether an animal
will adjust its handling location to improve vigilance. If
the benefits of vigilance during handling are high,
animals should not handle food items in locations where
vigilance is reduced if alternative locations that are more
favourable to vigilance are available. If the benefits of
vigilance during handling are low, either because the
ability to detect threats does not increase or because an
increased ability to detect threats does not increase fitness
(e.g. because the risk of attack is very low), animals should
handle food items where they are found. This is because
moving to another location increases the foraging time
and hence decreases the rate of gain of energy and
nutrients. Arenz & Leger (1997a, b, 1999a, b) showed
that thirteen-lined ground squirrels, Spermophilus tridecemlineatus, that were feeding on peanut butter in boxes that
restricted vigilance would emerge to scan, but it was not
possible for the squirrels to remove the food from the
boxes to handle it in a situation of better visibility. For
food items that can be carried, black-capped chickadees,
Poecile atricapillus, and grey squirrels will move to protective cover before handling (Lima 1985; Lima et al. 1985).
As far as we are aware, no one has examined whether animals will move to a location that allows improved vigilance before handling.
In this study, we test whether grey squirrels benefit from
vigilance while handling food items, by examining
whether they avoid handling in sites with limited visibility by moving to sites with better visibility. Arenz & Leger
(1997a, 1999a, b) found that thirteen-lined ground squirrels responded differently to lateral and overhead visual
obstruction, so we tested both situations. Like thirteenlined ground squirrels, grey squirrels are attacked by
both terrestrial and aerial predators, including dogs, Canis
familiaris, foxes, Vulpes vulpes and hawks (Long 1995;
Steele & Koprowski 2001). Lima (1985) and Lima et al.
(1985) found that handling time influenced the probability that chickadees and grey squirrels would carry items to
cover, as predicted by a model of the trade-off between
predation risk and foraging efficiency, so we tested small
items with a short handling time and large items with
a longer handling time.
METHODS
Experimental Apparatus
The apparatus consisted of a 112 124 75 cm
(W L H) frame constructed of 1 1-cm wood covered
by dark green tape. Each squirrel was presented with one
of three treatments: (1) lateral view obstructed (two sides
and one end of the frame covered with khaki-coloured
cloth), (2) overhead view obstructed (top of the frame
covered with cloth), or (3) control (a strip of cloth 5 cm
wide at the base of two sides and one end of the frame;
this was low enough for a squirrel to see over it). The
total area covered by cloth was 27 000 cm2 for lateral
obstruction, 13 888 cm2 for overhead obstruction and
1800 cm2 for the control. On the ground in the middle
of the apparatus, the experimenter placed a 14-cm diameter translucent brown glass plate. On the plate were
three crackers, each consisting of approximately 3 g of
a mixture of 17 parts peanut butter to 11 parts wheat
flour by weight sandwiched between two unsalted
soda crackers ðX SD ¼ 4:13 0:08 g; N ¼ 10Þ and five
sunflower seeds, Helianthus annuus, in their shells
ðX SD ¼ 0:09 0:02 g; N ¼ 12Þ. The crackers provided
a large item with a long handling time, and the sunflower seeds provided a small item with a short handling
time. Both items are attractive to squirrels and are consumed when found rather than scatter-hoarded (D. L.
Kramer & I. J. Makowska, unpublished observations). To
lead the squirrel to the plate, the experimenter made
a trail of eight sunflower seeds from the plate to another
MAKOWSKA & KRAMER: VIGILANCE IN SQUIRRELS
patch of five sunflower seeds at the open end of the
frame.
Protocol
We carried out trials between 0700 and 1500 hours
during 8e30 August and 3 Octobere13 November 2005 in
seven urban parks in Montreal, Canada. We selected
grassy locations with trees spaced about 3 m apart. To
avoid retesting the same individual, we moved at least
100 m between successful trials except on three occasions
where we moved a shorter distance because there were few
alternative locations and the large number of squirrels
made retesting unlikely. The apparatus was set up 1e2 m
from a tree large enough to provide a refuge (35 cm
diameter). Treatment order and orientation of the open
end (north, south, east, or west) were chosen randomly
and were unknown to the experimenter until a location
had been selected, except when a trial had to be repeated
(see below). A video camera (Sony Handycam, CCD-TR83
NTSC) on a 92-cm tripod was placed 10 m from the open
end. The experimenter enticed a squirrel to approach the
apparatus by throwing sunflower seeds. If more than one
squirrel approached, the others were distracted from the
apparatus by being given peanut butter crackers. A trial began when a squirrel contacted a food item on the plate
and ended when a squirrel approached the plate but left
the apparatus without picking up an item. Trials were
repeated using a different individual in a different location
if the focal squirrel was chased by a dog, directly approached by a human, or if another squirrel, a pigeon,
Columba livia, or a gull, Larus delawarensis, approached
to within 5 m of the apparatus. We completed 11 trials
of each of the three treatments.
We viewed the video recordings on a television to
determine handling location, occurrence of tail flagging,
handling times for all three crackers and the first three
seeds eaten from the plate, and moving times. Handling
location was classified as outside if the squirrel’s eyes were
out of the entrance of the apparatus during at least part of
the process, because this is the position that would result
in a large change in the visual field. In practice, most
squirrels emerged completely from the apparatus. The
rapid tail movements known as tail flagging, considered
an indicator of alarm (Horwich 1972; Gurnell 1987; Steele
& Koprowski 2001), were measured to determine whether
squirrels were more frightened by some treatments than
by others. Our criterion for tail flagging was at least 2 s
of lateral tail movements the first time that the squirrel
entered the frame. Handling time, measured with a stopwatch during real time viewing, was the time from the
start of oral contact of the food item until the initiation
of a downward movement of the forepaws. Moving was
the duration of forward locomotion to and from the handling location. Because the goal was to determine how
long it took to move out of the apparatus and back, only
trips without major interruptions to handle food or sniff
the ground were included.
Squirrels only carried crackers out of the apparatus. We
examined the effects of treatment and order (cracker
number) on the probability of carrying crackers using
a generalized linear mixed model (GLMM) in R (Faraway
2006). This test permits an unbalanced design, so we
included squirrels that ate only two crackers as well as
those that ate all three. Treatment, cracker number and
their interaction were treated as fixed effects and individual trial as a random effect. Individual trial was used to
avoid pseudoreplication problems associated with handling of several crackers by each squirrel. We used the
command glmmPQL with a binomial distribution and
a logit-link function (Faraway 2006). We compared the
squirrels’ responses to crackers and sunflower seeds using
Wilcoxon matched-pairs signed-ranks tests (Siegel &
Castellan 1988). We used the Fisher’s exact test (SYSTAT
10.2 SYSTAT, San Jose, California, U.S.A.) to compare the
effects of treatments on the occurrence of tail flagging. Although we had a priori predictions that the proportion of
items carried would increase with visual obstruction and
with larger items, other comparisons were made a posteriori, so we use two-tailed probabilities throughout for ease
of presentation.
RESULTS
Of the 33 squirrels, 27 ate all three crackers and six ate
only two crackers (N ¼ 2 squirrels in lateral obstruction;
N ¼ 1 in overhead obstruction; N ¼ 3 in the control).
Twenty-three of the 33 squirrels ate at least three seeds,
four squirrels ate one or two seeds (N ¼ 3 in lateral obstruction; N ¼ 1 in the control), and six squirrels ate
none (N ¼ 3 in lateral obstruction; N ¼ 3 in the control).
With lateral obstruction, squirrels carried all except one
cracker out of the apparatus for handling (Fig. 1a). Squirrels usually carried crackers 2e4 m from the apparatus
along the grass before handling, although some stopped
and handled crackers at the edge of the apparatus or
took them up a tree. With overhead obstruction and control treatments, only about one-third of the crackers were
carried out (overhead: 10/32; control: 10/30; Fig. 1b, c).
The number of crackers carried out differed significantly
between the lateral obstruction treatment and the control
treatment but not between the overhead obstruction
treatment and the control treatment (Table 1). Repeating
the analysis using the overhead treatment as the
comparison group showed that the lateral treatment
differed significantly from the overhead treatment (coefficient SE ¼ 3.509 0.940, t30 ¼ 3.732, P ¼ 0.0008). In
the control treatment, the proportion of crackers carried
decreased with successive crackers; this decrease was less
with overhead obstruction and absent with lateral obstruction (Fig. 1). The slope of the decrease differed between both the lateral obstruction treatment and the
control and between the overhead obstruction treatment
and the control, as indicated by significant interactions
in the GLMM (Table 1).
Squirrels never carried sunflower seeds out of the
apparatus for handling. For the eight squirrels in the
lateral obstruction treatment that handled at least one
sunflower seed, the mean proportion of crackers carried
out (1.0) was significantly greater than the mean
155
ANIMAL BEHAVIOUR, 74, 1
(a)
11
1
9
11
Table 1. Generalized linear mixed model analysis of the effect of lateral and overhead obstruction as compared to the control treatment
on the probability that grey squirrels would carry crackers outside
the apparatus for handling
Coefficient
0.8
Intercept
Lateral obstruction
Overhead
obstruction
Cracker number
Lateral obstruction*
cracker number
Overhead obstruction*cracker number
0.6
0.4
0.2
0
SE
df
t
P
0.263
2.850
0.659
0.638 57 0.413 0.681
0.937 30 3.041 <0.005
0.905 30 0.728 0.472
1.645
1.619
0.284 57 5.799 <0.0001
0.436 57 3.714 0.0005
0.852
0.383 57
2.225
0.03
(b)
1
Proportion carried out
156
0.8
0.6
11
0.4
11
10
0.2
0
(c)
1
0.8
0.6
11
0.4
of the apparatus between seed-handling events; this could
have provided some vigilance even though the squirrels
consumed the seeds within the apparatus. Of the 23 squirrels that ate three seeds, however, 14 ate them consecutively without leaving the apparatus. Nine of the 23
squirrels ate a cracker between seeds, but only three of
the squirrels handled the cracker outside (N ¼ 2 in lateral
obstruction; N ¼ 1 in the control).
Handling times averaged 150 s for a cracker and 5 s for
a seed. Average moving times were 3 s out and 11 s back.
Thus, moving out increased cracker handling time by an
average of 9%, whereas moving out would have increased
seed-handling time by an average of 280%.
Tail flagging occurred in 2 of 11 (18%) squirrels with
lateral obstruction, 4 of 10 (40%) squirrels with overhead
obstruction and 6 of 11 (55%) controls. Treatments were
not significantly different (Fisher’s exact test: lateral versus
control, P ¼ 0.18; overhead versus control, P ¼ 0.67; lateral versus overhead, P ¼ 0.36). There was also no association between tail flagging and handling location (Fisher’s
exact test: P ¼ 1.00, P ¼ 0.27 and P ¼ 0.22 for the first,
second and third cracker, respectively).
11
0.2
0
8
1
2
Cracker
3
Figure 1. Proportion of first, second and third crackers carried out of
the apparatus for handling in the (a) lateral obstruction, (b) overhead obstruction and (c) control treatments. Sample sizes for squirrels are given above bars.
proportion of seeds carried (0.0; Wilcoxon matched-pairs
signed-ranks test: T ¼ 36, N ¼ 8, P ¼ 0.0078). For the 11
squirrels in the overhead obstruction treatment, the difference between the proportion of crackers and the proportion of seeds carried approached significance (0.3
versus 0.0; T ¼ 15, N (number of not tied pairs) ¼ 5,
P ¼ 0.0625). For the controls, the eight individuals that
ate sunflower seeds carried a mean of 0.21 crackers and
0.0 seeds, but only three individuals differed in the
proportion of items carried, so we could not calculate a
P value. We also examined whether squirrels moved out
DISCUSSION
The grey squirrels’ response to lateral obstruction of their
view suggests that they are vigilant during semiupright
food handling. Squirrels carried nearly all crackers out of
the apparatus in the lateral obstruction treatment but only
about one-third of the crackers in the control treatment. If
vigilance did not occur during handling, we would expect
squirrels to consume the food where they found it, even if
their view was blocked, rather than taking the time to
change location before the start of handling. To gain
information about potential risks, animals might still
move out of the apparatus, but they should be as likely
to do this after handling a food item as before. It is not
clear why one-third of the controls moved out of the
apparatus. Some crackers may be carried because, even in
the control apparatus, the view could be improved, for
example, if a tree or other object partially obstructs the
animal’s view. There may be other explanations for
moving, such as a neophobic response to the apparatus
or an advantage to being closer to a tree (Lima 1985; Lima
MAKOWSKA & KRAMER: VIGILANCE IN SQUIRRELS
et al. 1985). Nevertheless, it is clear that lateral obstruction
increases the probability of moving as compared to the
controls, supporting an effect of visibility, even if it is
not the only factor. It is unlikely that this effect of lateral
obstruction was due to greater fear of this apparatus. Tail
flagging, a response to novel or fear-inducing situations
(Horwich 1972; Gurnell 1987; Steele & Koprowski 2001),
did not differ significantly between treatments and was,
in fact, least frequent in the lateral obstruction treatment.
The response to lateral obstruction observed in this study
is the first evidence to support the assumption (e.g. Lima
et al. 1985) that squirrels use the semiupright foodhandling posture for vigilance. Additional evidence comes
from a video analysis showing that squirrels searching for
sunflower seeds or feeding on peanut butter, activities that
occur in a quadripedal posture with the head down, show
higher rates of pausing than do squirrels handling sunflower seeds (T. Hackett, N. Sager & D. Kramer, unpublished observations). Thus, semiupright handling seems
to eliminate the need for head-raising vigilance that occurs in other activities. Our study supplements evidence,
summarized in the Introduction, indicating that vigilance
occurs during food handling with the head raised in three
species of finch and one primate (Lima 1988; Popp 1988;
Lima et al. 1999; Cresswell et al. 2003; Cowlishaw et al.
2004), although none have previously examined the response to visual obstruction. Neither our study nor others’
indicate whether vigilance is quantitatively lower during
food handling than during a head raise without food
handling.
Squirrels responded similarly to the overhead obstruction treatment and to the control. This result is similar to
studies by Arenz & Leger (1997a, b), who found that thirteen-lined ground squirrels feeding on peanut butter in
a clear plastic box would emerge for vigilance more often
when their lateral view was blocked than when their view
was not blocked or their overhead view was blocked. Although responses to overhead obstruction and no obstruction were similar, a subsequent study showed some effect
of overhead obstruction as well (Arenz & Leger 1999a).
Squirrels are killed by aerial predators (Temple 1987), so
not responding to blocking of the overhead view is not
likely to be due to the unimportance of this source of
risk. However, hawks typically use low, ground-hugging
flights when hunting highly visual prey like squirrels
(S. Lima, personal communication), so attacks from above
may be unlikely. Moreover, aerial predators are not
common in Montreal parks, and the species that are usually observed (Cooper’s hawk, Accipiter cooperii, and redshouldered hawk, Buteo lineatus) may not be a significant
threat to squirrels (J. Harrison, P. Bannon, personal
communication). On the other hand, dogs are frequently
present and often chase squirrels, foxes occur in some
parks, and squirrels may also need to watch for the approach of aggressive conspecifics. Thus, the differential response to lateral and overhead obstruction could be the
result of the relative lack of importance of aerial predation
at our study locations. Alternatively, overhead cover may
also reduce an aerial predator’s visibility of and access to
prey and thus be a form of protective cover that may compensate for the squirrels’ reduced visibility. In addition,
the lateral obstruction treatment limited escape routes
from terrestrial predators more than the overhead occlusion limited escape from either terrestrial or aerial predators, so it may be treated as a higher-risk location.
Squirrels carried crackers but not sunflower seeds out of
the apparatus. This result was not due to the squirrels’
inability to carry seeds, because we have observed squirrels
carrying sunflower seeds in their mouths in other situations, for example, when a dominant competitor arrived
at a patch. It is more likely that squirrels did not carry the
seeds because the nearly three-fold increase in time per
seed would have greatly reduced the rate of energy gain.
Similarly, Lima (1985) and Lima et al. (1985) showed that
the decision to carry food to a refuge for consumption depended on the size of the food item in chickadees and
squirrels. Arenz & Leger (1999a) also found that thirteen-lined ground squirrels decreased their vigilance
when the cost (due to a greater distance between vigilance
location and food source) increased.
Acknowledgments
This manuscript is based on an undergraduate research
project submitted to McGill University by I.J.M. The
McGill University Animal Care Committee approved the
research protocols (AUP 4942). We thank Gregory Makowski for his unique involvement at all stages of the
study. Talya Hackett and Mada Hoteit advised on field
methods and statistical analysis, respectively. Jeff Harrison
and Pierre Bannon provided information about birds of
prey in Montreal parks, René Marois advised on dual task
interference, Steve Lima shared observations on hawk
hunting tactics, and Luc-Alain Giraldeau suggested the
potential importance of escape route with overhead
occlusion. We are very grateful to Denis Réale for his
help with the GLMM and to Steve Lima and Carolyn Hall
for their comments on an earlier draft of the manuscript.
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