Behavioral Ecology
doi:10.1093/beheco/arp035
Advance Access publication 13 April 2009
Theory successfully predicts hiding time: new
data for the lizard Sceloporus virgatus and a review
William E. Cooper Jr
Department of Biology, Indiana University–Purdue University Fort Wayne, Fort Wayne, IN 46805, USA
Economic hypotheses predict that prey in refuges after short-term encounters with predators decide how long to hide before
emerging (hiding time) based on cost of emerging (predation risk) and cost of not emerging. Here, I report tests of predictions
of these hypotheses for several cost of emerging and cost of remaining in refuge factors in the lizard Sceloporus virgatus by
approaching lizards to elicit refuge entry, review tests of the predictions to evaluate the success of current models in predicting
hiding time, and note parallels between models predicting hiding time and flight initiation distance (distance separating
predator from prey when escape begins). Hiding times were longer under greater risk implied by faster, more direct, and
repeated approaches and by greater proximity of the predator to the refuge during hiding. Lizards responded to costs of refuge
use by emerging sooner when food was visible outside and when the refuge was substantially cooler than the lizard. In addition,
lizards were more likely to enter refuges when approached rapidly and when cloudiness precluded effective thermoregulation by
basking. Review of findings for lizards and other taxa revealed strong support for the predictions of cost-benefit models that
hiding time increases with cost of emerging and decreases with cost of staying in refuge. Examination of parallel predictions by
escape theory and refuge use theory emphasizes their fundamental similarity and led to identification of an untested prediction
of refuge use theory. Key words: emergence time, escape theory, hiding time, predation risk, refuge use, Squamata, thermal
cost. [Behav Ecol 20:585–592 (2009)]
rey that use refuges to escape during short-term encounters
with predators must decide when to emerge. Hiding time
(HT ¼ emergence time), the interval spent in a refuge between entry and emergence, is affected by many factors that
influence predation risk upon emerging (cost of emerging)
and cost of continuing to hide. Refuge use theory predicts
HT from the balance of risk with hiding cost (Martı́n and
López 1999a; Cooper and Frederick 2007a). Hiding costs include lost social and feeding opportunities and thermal cost
of decreasing body temperature in refuge for ectotherms.
Time spent hiding after encounters with predators is adjusted
to degree of risk upon emergence (Dill and Gillett 1991;
Scarratt and Godin 1992; Blumstein and Pelletier 2005) and
to cost of hiding, including opportunity costs (Koivula et al.
1995; Dill and Fraser 1997) and physiological costs such as
oxygen deficit (Wolf and Kramer 1987) and decreasing body
temperature in ectotherms (Martı́n and López 1999a). Thus,
decisions about HT are believed to be based on trade-offs
between cost of emerging and cost of remaining in refuge.
The first cost-benefit approaches to HT are extensions of escape theory (Ydenberg and Dill 1986; Cooper and Frederick
2007b). Flight initiation distance (FID ¼ distance between
predator and prey when escape begins) increases as predation
risk (cost of not fleeing) increases and decreases as cost of
escape (e.g., lost social and foraging opportunities) increases.
In models of HT, cost of emerging (risk) corresponds to cost
of not fleeing and cost of hiding corresponds to cost of escape. One model of HT predicts emergence when cost of
emerging equals cost of hiding (Martı́n and López 1999a);
another shows that prey can do better by emerging at a time
that maximizes expected fitness (Cooper and Frederick
2007a). The predictions are equivalent to predictions that
P
Address correspondence to W.E. Cooper. E-mail: cooperw@ipfw.
edu.
Received 3 July 2008; revised 16 January 2009; accepted 17
February 2009.
The Author 2009. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
escape begins when costs of fleeing and not fleeing are equal
(Ydenberg and Dill 1986) or expected fitness is maximized
(Cooper and Frederick 2007b). Quantitative measures of effects of risks and costs on fitness would greatly facilitate evaluation of the models but have not been done. Predictions of
both models are usually tested at the ordinal level, but most
predictions of the models at this level are identical. Both predict, for example, that HT increases as intensity of factors
affecting risk upon emergence increase and decreases as cost
of staying in refuge increases. Prey in refuge and their predators may play waiting games in which the behavior of each
affects that of the other (Hugie 2003). Economic considerations apply to waiting games and to cases in which predators
move elsewhere quickly after prey enter refuges.
Theory adequately predicts HT for risks including predator
abundance, approach speed, directness of approach, and persistence and prey proximity to refuge (Scarratt and Godin 1992;
Sih 1992; Cooper 1998; Martı́n and López 1999a, 2000, 2001;
Martı́n et al. 2005), body size, and escape ability (Krause et al.
1998; Krause, Longworth, and Ruxton 2000; Cooper and Wilson,
forthcoming; Cooper WE Jr and Wilson DS, unpublished data).
As predicted, prey emerge sooner if cost of continued hiding is
greater, for example, when hungry, body condition is low or food
is present; when staying in refuge entails loss of opportunities to
court or engage in aggressive behavior; or when body temperature decreases, oxygen concentration is reduced or predators are
present in refuge (Wolf and Kramer 1987; Dill and Gillett 1991;
Sih 1992; Dill and Fraser 1997; Krause et al. 1998; Dı́az-Uriarte
1999; Martı́n and López 1999a, 1999b, 2003; Krause, Cheng, et al.
2000; Amo et al. 2003, 2004a, 2004b, 2006, 2007; Jennions et al.
2003; Martı́n et al. 2003a, 2003b; Blumstein and Pelletier 2005;
Polo et al. 2005; Petrie and Ryer 2006; Reaney 2007).
HT has been studied most extensively in lizards (references
above) but in very few species. These are a single skink (Cooper
1998), 2 lacertids (e.g., Martı́n and López 1999a; Amo et al.
2003), a tropidurid (Dı́az-Uriarte 1999), and a phrynosomatid
(Cooper and Wilson, forthcoming). Our knowledge is fragmentary and the degree of variation in effects among taxa is
Behavioral Ecology
586
unknown. We know little about effects of multiple risks and
costs operating simultaneously.
I studied effects on HTof factors influencing costs of emerging
and not emerging in the striped plateau lizard, Sceloporus virgatus. Several factors affect FID in S. virgatus (Cooper 2005, 2007;
Cooper and Wilson 2007a, 2007b; Cooper WE Jr and Wilson DS,
unpublished data), but only tail loss and refuge temperature
are known to affect HT (Cooper and Wilson Forthcoming). HT
increases after tail loss because running speed is reduced and
autotomy cannot be reused until the tail has regenerated
(Ballinger et al. 1979; Punzo 1982; Cooper and Wilson, forthcoming; Cooper WE Jr and Wilson DS, unpublished data). It
decreases when refuges are cooler than body or outside air
temperature (Cooper and Wilson, forthcoming), presumably
because sprint speed decreases as body temperature decreases
(Bennett 1980), increasing predation risk and decreasing efficiency of foraging and social behavior (Martı́n and López
1999a).
I present experimental evidence for effects on refuge use of
four cost of emergence factors and two cost of hiding factors
in S. virgatus. Because greater predation threat is implied by
greater approach speed, more direct approach, closer proximity of a predator to the refuge, and persistence of the
predator manifested by repeated attack, I predicted that
HT is greater for greater approach speed, more direct approach, closer proximity, and the second of two attacks. Because prey staying in refuge when food is present may lose
opportunities to eat, briefer HT is predicted when food is
present. Because ectothermic prey in refuges cooler than
body temperature progressively lose body heat, HT is shorter
when temperature is lower than outside (e.g., Martı́n and
López 1999a, 1999b). For heliothermic lizards that bask to
raise body temperature, the difference between body and
refuge temperature should be greater in sunny conditions
than when cloud cover greatly reduces basking efficiency,
provided that air temperature is less than preferred body
temperature. I predicted that the temperature difference is
greater than in cloudy than sunny conditions. Because thermal cost of entering and remaining in refuge increases with
difference in body and refuge temperatures (Martı́n and
López 1999a, 1999b; Cooper and Frederick 2007a), I predicted that likelihood of entering refuge is greater in cloudy
than sunny conditions.
side of a tree trunk), and in the others, I continued approaching until it entered a crevice refuge. I wore clothes of similar
muted color each day. Human investigators are commonly
used to induce escape and refuge entry. Use of this method
is convenient and has allowed verification of many predictions from escape theory, and refuge use theory based on
magnitudes factors that affect predation risk and costs of fleeing or remaining in refuge (reviewed by Stankowich and
Blumstein 2005; Cooper and Wilson 2007b). One drawback
of this method is that certain prey species exhibit predatorspecific antipredatory behaviors (Stuart-Fox et al. 2006).
However, no differences in types of escape behavior or refuge use were apparent in pilot tests of reactions by S. virgatus
to approaches by a mounted Cooper’s hawk (Accipiter cooperii) having widely spread wings, a model snake, and a human
investigator (Cooper, forthcoming).
Before each trial, I walked very slowly through the study site
searching visually for lizards. Upon detecting an adult lizard, I
continued to move slowly until I was approximately 5 m from
the lizard, and then oriented directly toward it and stopped
moving briefly before commencing a trial. When a lizard entered refuge, I withdrew to a position 5 m from the opening
of the crevice until a lizard emerged. In experiments requiring
a second approach, I then began from 5 m again except in the
studies of effects of predator proximity and presence of food.
Starting distance, the distance between predator and prey
when escape begins, affects FID, the distance between predator
and prey when escape begins, in some prey (e.g., Blumstein
2003; Cooper 2005; Stankowich and Coss 2006). In S. virgatus,
starting distance does not affect FID during slow approaches
and has only a minor effect during fast approaches (Cooper
2005). Whether starting distance affects HT is unknown, but
the design required to standardize testing in the experimental
conditions removed starting distance as a potential source of
variation.
Pseudoreplication was avoided by 1) using repeated measures designs and continuously monitoring the individual between trials, 2) walking through each area only once during
an experiment, and 3) starting the next trial when the location
of the previously tested lizard was known or moving at least 30
m along a transect before conducting another trial. After
breaks in data collection, I began at least 100 m from the location of the previous test to an area where no data had been
collected during that experiment. Some individuals were
tested in more than one experiment.
METHODS
Animals, study site, and experimental approach
Experimental design
Sceloporus virgatus is a phrynosomatid ambush forager that is
active on the ground, rocks, and logs and low on tree trunks.
It escapes by running away, running longer distances when it
can run up slopes (Cooper and Wilson 2007a), or by entering
refuges. The most common refuges are crevices beneath rocks
and the far side of tree trunks, but lizards also hide under logs
and grass clumps (Cooper and Wilson 2007a).
I conducted experiments on factors affecting refuge use by
S. virgatus in the Chiricahua Mountains of southeastern Arizona
in May 2004 before the breeding season began. All work was
done in the western branch of the Coronado National Forest at
an elevation of approximately 1800 m. Habitats there were open
forest and a rocky creek bed. With the exception of a single
experiment in which effects of cloudiness were studied, all observations were made on sunny days with light or no breeze
between 0930 and 1530 h after morning basking had been
completed and lizards were fully active.
I elicited entry into refuge by simulating an attacking predator by approaching until a lizard fled. In one study, I stopped
to record whether it would enter refuge (rock crevice or far
Approach speed
Lizards were approached directly using two practiced walking
speeds. The slow speed was 33.7 6 0.9 m/min (n ¼ 10; data
here and throughout are presented as X 6 standard error);
the fast speed was 125.1 6 1.8 m/min (n ¼ 10). Approach
speeds were practiced daily to ensure consistency. In one experiment, I stopped moving as soon as a lizard began to flee in
order to assess the effect of approach speed on probability of
entering a refuge. Intertrial intervals were 1 min if a lizard did
not enter refuge or the duration of hiding plus 1 min after
emergence if the lizards entered refuge, although carryover
effects of risk in the previous trial might have been larger than
if longer intertrial intervals had been used, especially when
the first approach was fast. However, hiding prey respond to
risk implied by a predator’s current as well as its behavior in
the recent past (Martı́n and López 2003). Unless previous
predator behavior has an overwhelming effect, counterbalancing the trial sequence should allow detection of responses to
different risk levels associated with different approach speeds,
even at short intertrial intervals. In practice, short intertrial
Cooper • Risk, cost, and refuge
intervals have worked well in studies of HT in lizards (e.g.,
Cooper 1998; Martı́n and López 2001; Cooper et al. 2003).
A lizard was recorded as entering refuge (hiding) if it fled to
the far side of a tree trunk or into a rock crevice. In the other
experiment, I continued to approach each individual until it entered a rock crevice and recorded the HT, which was time in
seconds from initial entry until the lizard’s entire body emerged
from the refuge. If the lizard did not emerge after 10 min, the
trial was terminated and HT was recorded as 600 s in this and the
other experiments. When a lizard did not emerge within 600 s in
its first trial, I withdrew to a greater distance to hasten emergence, and then repeated the procedure used during the initial
approach 1 min after the lizard emerged. Intertrial intervals
were HT plus 1 min in this and the studies describe below.
The order of trials was counterbalanced among lizards to prevent sequential bias in all studies using repeated measures
designs except the study of predator persistence.
Directness of approach, predator proximity and persistence, and
foraging opportunity
To study effects of directness of approach on HT, lizards were
approached at the faster approach speed either directly or indirectly along a straight path that bypassed them by 1 m. To
study effects of a predator’s proximity to the refuge while visible to a lizard looking out of it, I approached a lizard at the
faster speed and then stood facing the opening of the crevice at
a distance of either 1 m or 8–10 m. To study effects of predator
persistence on HT, I slowly approached a lizard until it entered
refuge, withdrew 5 m, recorded its HT, waited 1 min, and then
repeated this procedure using the same approach speed.
To study effects of the presence of food outside refuge on
HT, I approached at the faster speed. When a lizard entered
refuge, I placed a tethered living cricket or tethered stick of
similar proportions 1 m in front of the crevice opening where
it could be seen by the lizard. Crickets and sticks were tied by
string to a fishing rod used to position them while I stood in
front of the crevice about 2.3 m past the cricket.
Thermal cost of refuge use
I studied the effect of cloudy conditions that limit opportunity
to achieve preferred body temperature by basking on the probability of entering refuge. In S. virgatus, the mean field body
temperature of active lizards is 33.4 C and the maximum is
39.3 C (Smith and Ballinger 1994). I collected data in a restricted range of air temperatures, 26.0–28.2 C, well below
body temperatures of active lizards that have completed basking. At these temperatures, I slowly approached lizards in full
sun and lizards in exposed positions when cloud cover had
persisted for at least 20 min. Lizards were recorded as entering refuge, remaining in view, or fleeing out of sight on the far
sides of rock without entering a crevice. I approached another
group of lizards close to rocks that were small enough to move
easily and had crevices suitable for use as refuges. When
a lizard had entered the refuge, I recorded the refuge temperature to the nearest 0.1 C, and then turned the rock over,
captured the lizard by hand, and measured its body temperature to the nearest 0.1 C using a Schultheis quick-reading
cloacal thermometer. If a lizard approached a crevice and
stopped adjacent to, but outside it, I captured the lizard, measured its body temperature, and then measured the air temperature in the refuge. Lizards that entered refuges thus
could begin cooling during the approximately 15 s taken to
measure refuge temperature. However, any slight decrease in
body temperature during that time would have only a very
small effect compared with the large differences observed
between conditions, whereas moving the rock to catch the
lizard as quickly as possible is likely to have had a much larger
effect on air temperature in the crevice after the rock had
587
been restored to its former position. If body temperatures
of lizards in cloudy conditions had been the same as those
in sunny conditions before entering refuges, they would have
cooled by only less than one degree in the brief time because
they entered refuge (Bartholomew 1982), which would have
had no impact on the interpretations of results.
Analysis
Repeated measures designs were used in all experiments except
those on thermal cost of refuge use. The difference in frequency
of refuge entry between approach speeds significance using
a McNemar’s test. For experiments using repeated measure
designs, differences in HT between experimental conditions
were examined by randomized blocks analysis of variance.
The assumptions of analysis of variance regarding homogeneity
of variance and normality were verified using Hartley’s Fmax tests
and Kolmogorov–Smirnov tests, respectively. When significant
heterogeneity of variance occurred, data were subjected to logarithmic or square root transformation as needed to obtain
homogeneous variances. When variances remained significantly heterogeneous after both transformations, data were analyzed using Wilcoxon matched-pairs signed-ranks tests.
Sign tests were conducted to gage differences in frequencies
of between conditions in studies of approach speed, predator
proximity, predator persistence, and presence of a cricket outside the refuge. The difference in proportions of lizards that
entered refuge in sunny and cloudy conditions was assessed
by a Fisher’s Exact probability test. The differences between
sunny and cloudy conditions for the difference between body
and refuge temperature was tested for significance using
a Mann–Whitney U test.
All statistical tests were 2-tailed, with a ¼ 0.05. Cohen’s d is
used to present effect sizes, that is, measures of the degree to
which the null hypothesis is falsified by the statistical test, for
comparisons involving means and standard deviation. Values
of d corresponding to small, medium, and large effects are
0.20, 0.50, and 0.80, respectively (Cohen 1992). Cohen’s d applies to independent
groups; affi modified version for repeated
pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
measures is drm ¼ t 2ð12rÞ=n; where r and t have their usual
statistical interpretations, r being the correlation between first
and second trials (Cortina and Hossein 2000). For sign tests,
the effect size is g ¼ P 2 0.50, with small, medium, and large
effects being 0.05, 0.15, and 0.25, respectively, with maximum
value 0.50 (Cohen 1992). For the Mann–Whitney U test, effect
size is U divided by the product of the two sample sizes (Newcombe 2006). The statistic requivalent, which is based on point
biserial correlation, was used as the effect size for the Fisher’s
Exact test and McNemar’s test (Rosenthal and Rubin 2003).
RESULTS
Risk factors
Approach speed
When the investigator stopped moving as soon as a lizard fled,
12 individuals entered refuges after fast but not slow
approaches, 3 entered after both approaches, 3 entered after
neither approach, and 2 entered after slow but not rapid approach. Lizards were significantly more likely to enter refuges
when approached rapidly than slowly (McNemar’s test,
v21 ¼ 5:79; P ¼ 0.016; requivalent ¼ 0.55).
After approach continued until lizards entered refuges, HT
was significantly longer following fast than slow approaches (Table 1; F1,11 ¼ 14.80, P ¼ 0.0027; drm ¼ 1.00). Variances were
homogeneous (Hartley’s Fmax2;11 ¼ 2:61; P . 0.05), and the
distributions did not depart significantly from normality (slow:
Kolmogorov–Smirnov d ¼ 0.23, P . 0.05; fast: d ¼ 0.10,
Behavioral Ecology
588
Table 1
HTs (s) for Sceloporus virgatus in several experiments on factors
affecting costs of merging and costs of remaining in refuge
Risk or condition
or cost or group X
Approach speed
Slow
Fast
Directness of
approach
Direct
1 m bypass
Predator
proximity
1m
8–10 m
Predator
persistence
First approach
Second
approach
Cricket presence
Present
Absent
Standard
error
Range
122.8 33.7
290.8 54.4
264.6 65.4
97.9 39.3
255.8 54.7
102.5 24.0
N
Effect
size (d) P
1.00
0.0027
0.79
0.0022
0.83
0.0008
1.40
0.0012
2.25
5.9 3 1025
14–396 12
27–600 12
47–600 12
20–436 12
9–600 14
16–235 14
57.4 22.1
174.5 42.3
3–328 17
6–600 17
23.6 8.5
260.0 58.1
2–115 13
42–600 13
P . 0.05). HT was longer after fast approaches for 11 of 12
individuals (sign test, P ¼ 0.0094; g ¼ 0.49).
Directness of approach
All 12 individuals hid longer after direct than indirect approach. Three individuals did not emerge before the ends
of their 600 s trials when approached directly. Although the
distribution of HT did not depart significantly from normality
(d ¼ 0.19, P . 0.05), I analyzed the data nonparametrically to
be conservative. HT was significantly longer following direct
approaches than indirect approaches with 1 m minimum bypass distance (Table 1; Wilcoxon matched-pairs signed-ranks
test, T12 ¼ 0.0, P ¼ 0.0022; drm ¼ 0.79).
Proximity of predator to the refuge
Thirteen of 14 individuals had longer HTs when the predator
stood 1 m from the refuge than 8–10 m from the refuge (sign
test, P , 0.0020; g ¼ 0.498). Variances of the raw data were
significantly heterogeneous (Fmax2;13 ¼ 5:21; P , 0.01), but
variances of logarithmically transformed data were homogeneous (Fmax2;13 ¼ 1:21; P . 0.05). The distributions of HT did
not depart significantly from normality for transformed near
(d ¼ 0.11, P . 0.05) or far (d ¼ 0.19, P . 0.05) data. HT was
significantly longer when I stood nearer the refuge (Table 1;
F1,13 ¼ 19.16, P , 0.00075; drm ¼ 0.83).
data were significantly heterogeneous (Fmax2;12 ¼ 46:50; P ,
0.01), but variances of logarithmically transformed data were
homogeneous (Fmax2;12 ¼ 1:17; P . 0.05). Distributions of the
transformed data did not depart significantly from normality
(cricket: d ¼ 0.13, P . 0.05; no cricket: d ¼ 0.16, P . 0.05).
HT was much shorter in the presence of a cricket and significantly so (Table 1; F1,12 ¼ 32.43, P ¼ 5.9 3 10-5; drm ¼ 2.25).
Thermal costs
At air temperatures of 26.0–28.2 C, lizards entered refuges
much more frequently in cloudy than sunny conditions. In
cloudy conditions, 21 of 27 individuals entered refuges, 4
remained in view, and 2 fled to far sides of rocks without entering a crevice. In sunny conditions, 4 entered refuges, 12
remained in view after fleeing, and 2 fled to the far sides of
rocks without entering refuge. Pooling data for lizards that
remained in view or outside refuges on the far side of rocks,
lizards were significantly more likely to enter refuges in cloudy
than sunny conditions (Fisher’s P ¼ 0.0049; requivalent ¼ 0.65).
Variances of raw difference between body temperature and
refuge temperature were significantly heterogeneous
(Fmax2;24 ¼ 3:30; P ¼ 0.045), but the square root transformed
data had homogenous variances (Fmax2;24 ¼ 1:03; P . 0.05). In
both sunny and cloudy conditions, body temperature was
warmer than refuge temperature in all individuals. Thus, body
temperature was significantly warmer than refuge temperature in each group (sign tests—sunny: P ¼ 0.00098, n ¼ 11,
g ¼ 0.499; cloudy: P ¼ 6.1 3 1025, n ¼ 15, g ¼ 0.500). The
difference between body and refuge temperatures was significantly greater in sunny than cloudy conditions (Figure 1,
F1,24 ¼ 52.29, P , 1.0 3 1026; Cohen’s d ¼ 2.95).
DISCUSSION
Refuge use by S. virgatus and similarity of cost-benefit
assessment in escape and refuge use
Sceloporus virgatus adjusted HT to several factors that indicate
costs of emerging and remaining in refuge. Findings for each
factor and all factors collectively strongly support cost-benefit
hypotheses of HT (Martı́n and López 1999a; Cooper and
Frederick 2007a). Each factor had a large effect size, showing
that lizards make large adjustments of HT to current levels of
predation risk and cost of remaining in refuge.
Predator persistence
Fourteen of 17 individuals hid longer before emerging after
the second approach than the first (sign test: P ¼ 0.015,
g ¼ 0.485). Variances were significantly heterogeneous for raw
data (Fmax2;16 ¼ 3:67; P , 0.05), but were homogeneous for
logarithmically transformed data (Fmax2;16 ¼ 1:08; P . 0.05).
Distribution of transformed data did not depart significantly
from normality (first approach: d ¼ 0.14, P . 0.05; second
approach: d ¼ 0.13, P . 0.05). Using transformed data, HTs
were significantly longer following second than first approaches
(Table 1; F1,16 ¼ 15.32, P ¼ 0.0012; drm ¼ 1.40).
Costs of refuge use
Food outside refuge
All 13 lizards emerged after shorter HTs when a cricket was
present (sign test, P ¼ 0.0024, g ¼ 0.498). Variances of raw
Figure 1
Differences between body and refuge temperatures (C) for
Sceloporus virgatus in sunny and cloudy conditions. Error bars
represent 1.0 standard error.
Cooper • Risk, cost, and refuge
589
Table 2
Effects of factors that influence risk of predation upon emerging from refuge and costs of remaining in refuge on HT in lizards
Species
Factor
Costs of emerging (risk)
Approach speed (AS)
Approach directness (AD)
Proximity to refuge (PR)
Persistence (PP)
Prey risk factor
Tail loss
Costs of hiding
Food near refuge (FN)
Body condition (BC)
Male near refuge (MN)
Female near refuge (FN)
Thermal cost (TC)
Predator in refuge
Effect on HT
SV
HT
HT
HT
HT
X
X
X
X
[ as
[ as
[ as
[ as
AS [
AD [
PR [
PP [
HT . after
X
HT
HT
HT
HT
HT
HT
X
Y if FN
Y as BC Y
Y if MN
Y if FN
Y as TC [
Y if present
TH
PL
IC
PM
References
X
X
X
X
X
X
X
X
X
1–4
1, 3, and 5
1, 4, and 6
1–2 and 7–10
X
X
11
X
X
X
X
X
X
X
X
1 and 12
13
14
15
5–7 and 16–18
19–20
Thermal costs is body temperature or outside temperature minus refuge temperature. SV, Sceloporus virgatus; TH, Tropidurus hispidus; PL, Plestiodon
laticeps; IC, Iberolacerta cyreni; PM, Podarcis muralis. 1, This paper; 2, Cooper (1998); 3, Cooper et al. (2003); 4, Martı́n and López (2004); 5, Martin
and López (1999a); 6, Martı́n and López (2005); 7, Martin and López (2001); 8, Polo et al. (2005); 9, Martin and López (1999b); 10, Amo et al.
(2006); 11, Cooper WE Jr and Wilson DS (unpublished data); 12, Martı́n et al. (2003a); 13, Amo et al. (2007); 14, Diáz-Uriarte (1999); 15, Martin
et al. (2003b); 16, Amo et al. (2003); 17, Amo et al. (2004a); 18, Cooper and Wilson (forthcoming); 19, Amo et al. (2004b); 20, Amo et al. (2006).
Lizards hide more frequently and longer for faster approach. They have longer FID and some flee farther when
approached more rapidly (e.g., Martı́n and López 1996;
Stankowich and Blumstein 2005). The common threat is that
FID, refuge entry, and HT increase as assessed risk increases.
Similarly, HT and FID increase as approach becomes more
direct and is repeated, that is, as risk increases. The effect of
predator proximity on HT has a parallel effect for escape: FID
increases with distance to refuge (Bulova 1994; Cooper 1997b,
2000b). HT and FID decrease if food or breeding conspecifics
are present, that is, when cost fleeing or hiding increases (e.g.,
Burger and Gochfeld 1990; Cooper 1997a, 1999, 2000a;
Cooper and Pérez-Mellado 2004).
Theories of FID (Ydenberg and Dill 1986; Cooper and
Frederick 2007b) and HT (Martı́n and López 1999a; Cooper
and Frederick 2007a) make parallel predictions about costs
and benefits that correspond to empirically observed parallels
between escape and refuge use. The congruency of effects of
predation risk and costs of escaping or not emerging on FID
and HT suggests that mechanisms of assessing costs and benefits used to make decisions about escape behavior and continued occupation of refuges are in many respects identical or
very similar.
FID in some lizards increases as body temperature decreases
because cool lizards are slower runners, increasing predation
risk (Rand 1964; Smith 1997). No parallel effect is known for
refuge use, but warm lizards emerging sooner from cooler
refuges to minimize decrease in body temperature. A cool,
slow lizard already in refuge faces greater risk upon emerging,
leading to the untested prediction that lizards cool enough to
be slow should be more reluctant to emerge in the face of risk,
such as a nearby predator, than warmer lizards. For cooler
lizards, cost of emerging is greater due to slower speed and
cost of hiding is lower due to reduced efficiency of foraging or
social behavior. Longer HT for cooler lizards is predicted both
by greater cost of emerging and lower cost of not emerging.
Factors affecting HT may also affect probability of entering
refuge: S. virgatus entered refuges more frequently when approached rapidly than slowly (replicating Cooper, forthcoming) and repeatedly (Cooper, forthcoming) and were more
reluctant to enter refuges in sunny conditions permitting
effective thermoregulation by basking than in cloudy conditions.
Similar findings have been reported for other lizards (approach
speed—Cooper 1997c; repeated approach—Martı́n and López
2003; temperature—Cooper 2000b, 2003; and autotomy—
Cooper 2007).
Factors affecting HT in lizards and other taxa
Findings for S. virgatus and other lizards indicate that phylogenetically and ecologically diverse species respond similarly
to the factors. Species for which the most factors affecting HT
have been studied (Table 2) are S. virgatus, a terrestrial ambush forager belonging to Iguania, 1 of the 2 major clades of
squamate reptiles, and 2 representative of the other major
clade, Scleroglossa. The scleroglossans are an actively foraging
semiarboreal skink Plestiodon laticeps (Cooper et al. 2001), and
the lacertids Iberolacerta cyreni and Podarcis muralis, active foragers but much less active than P. laticeps (Verwaijen and Van
Damme 2008).
Consistency across taxa is striking. HT increases as predator
approach speed, directness of approach, predator proximity to
refuge, and predator persistence increase (Table 2). HT increases after tail loss due to autotomy, which decreases running
speed, increasing risk of predation (Cooper and Wilson, forthcoming; Cooper WE Jr and Wilson DS, unpublished data). HT
decreases as costs of remaining in refuge increase in all studies:
It decreases as trophic and thermal costs of hiding increase, in
the presence of male and female conspecifics when social opportunities might be lost by remaining in refuge and when
predation risk is present in the refuge (Table 2).
Studies of non-lizard taxa (Table 3) provide information
about taxonomic breadth of effects of factors studied in lizards and others not studied in lizards as well as providing
a basis (with Table 2) for evaluating the generality of success
of cost-benefit models in predicting HT. Several factors have
similar effects on HT in lizards and other taxa: HT increases
with directness of approach and proximity of a predator (fiddler crab, the effect for directness is marginal, Jennions et al.
2003), predator persistence (turtle, Martı́n et al. 2005). HT
decreases in males when females are present outside the refuge (fiddler crab, Reaney 2007) and when food is available
Behavioral Ecology
590
Table 3
Effects of factors that influence risk of predation upon emerging from refuge and costs of remaining in refuge on HT in non-lizard taxa
Factor
Effect on HT
Species
Minnow
Stickleback
Marmot
Phoxinus phoxinus
Gasterosteus aculeatus
Marmota flaviventris
Krause, Cheng, et al. (2000)
Krause, Cheng, et al. (2000)
Rhoades and Blumstein (2007)
Approach directness (AD)
Proximity to refuge (PR)
when detected
Persistence (PP)
HT . when approach
HT . when approach
HT [ and AS [ only for fast
approaches, AS and food
presence interact
HT [ as AD [
HT [ as PR [
Fiddler crab
Fiddler crab
Uca lactea perplexa
U. l. perplexa
Jennions et al. (2003)
Jennions et al. (2003)
HT [ as PP [
Turtle
Martı́n et al. (2005)
Duration of handling (DH)
HT [ as DH [
Hermit crab
Turtle
Field crickets
Mauremys leprosa
on land
Pagurus acadianus
M. leprosa on land
Gryllus spp.
Scarratt and Godin (1992)
Martı́n et al. (2005)
Kortet et al. (2007)
Polychaete
Fiddler crab
Serpula vermicularis
Uca mjoebergi
Dill and Fraser (1997)
Reaney (2007)
Hermit crab
Marmot
Scarratt and Godin (1992)
Blumstein and Pelletier (2005)
Costs of emerging (risk)
Predator approach
Approach speed (AS)
Parasitism (PA)
Costs of hiding
Food near refuge (FN)
HT [ as PA [
HT Y if FN [
HT Y as FN [
During foraging period
No effect on HT
HT Y as FN [
For slow AS only
HT [ if FN [
References
Interaction with approach
speed (see AS above)
HTY as H [
HTY as H [
HTY as H [
HTY as H [
HTY if FN
HT[ as BS [
HT[ as BS [
HT[ as BS [
Marmot
P. acadianus
M. flaviventris
Bold individuals
M. flaviventris
Shy individuals
M flaviventris
Barnacle
Minnow
Stickleback
Willow tit
Fiddler crab
Fiddler crab
Minnow
Stickleback
Balanus glandula
P. phoxinus
G. aculeatus
Parus montanus
U. mjoebergi
U. l. perplexa
P. phoxinus
G. aculeatus
Land versus water
HT[ as BS [
HT . on land
Marmot
Turtle
Low dissolved O2 (DO)
HT[ as DO [
Clam
M. flaviventris
M. leprosa turned
on carapace
Corbicula fluminea
Hunger (H)
Female near refuge (FN)
Body size (BS)
outside the refuge (polychaete worm, Dill and Fraser 1997;
fiddler crab: Reaney 2007; and bold individuals of yellowbellied marmots: Blumstein and Pelletier 2005).
Relationships of two findings to theoretical predictions are
less obvious. Size of food items near a hermit crab’s shell refuge
did not affect HT (Scarratt and Godin 1992). This result is
consistent with predictions because all items were larger than
could be eaten entirely. That HT increased in shy yellowbellied marmots (individuals that had very long FIDs) when
food was near refuges (Blumstein and Pelletier 2005) poses
a challenge to cost-benefit models. This finding would be
consistent with theory if presence of food, its placement there
by investigators, and/or human scent on the food or near the
refuge increased perceived risk more for shy than bold marmots. Another hypothesis is that individuals with shorter FID
were hungrier or had poorer body condition than those having longer FID, whereas the latter assessed the food as a harvestable asset that would reduce foraging costs upon
emergence, permitting longer HT.
Effects of several factors studied only in lizards or in groups
other than lizards also verify predictions for HT based on costbenefit models. Factors studied only in lizards are tail loss, thermal cost, and presence of a rival male near refuge or a predator
in the refuge.
Factors studied only in non-lizard taxa are approach (2 fish),
duration and intensity of handling by the predator (turtle),
Marmot
Blumstein and Pelletier (2005)
Rhoades and Blumstein (2007)
Dill and Gillett (1991)
Krause, Cheng, et al. (2000)
Krause, Cheng, et al. (2000)
Koivula et al. (1995)
Reaney (2007)
Jennions et al. (2003)
Krause, Cheng, et al. (2000)
Krause et al. (1998) and Krause,
Cheng, et al. (2000)
Blumstein and Pelletier (2005)
Martı́n et al. (2005)
Saloom and Duncan (2005)
exposure to parasitism (cricket), hunger (a barnacle, 2 fish,
and a bird), body size (a crab, 2 fish, and a mammal), habitat
(land vs. water in a turtle), and dissolved oxygen concentration
(a clam). The effects of these factors are all consistent with predictions based on costs and benefits, with a possible exception
below for approach speed.
Only effects of approach speed and body condition differ
among taxa. In lizards, HT increased with the predator’s approach speed (Table 2), but in yellow-bellied marmots (Table
3), approach speed interacted with presence of food near the
refuge (Rhoades and Blumstein 2007). HT did not differ between approach speeds when food was present or absent, but
a marginal 3-way interaction between approach speed, food
presence, and the distance from the approaching investigator
when marmots entered burrows (Rhoades and Blumstein
2007) hints that differences in boldness among individuals
may modify effects of approach speed and food presence.
These findings contradict simple predictions about the effect
of approach speed on HT and suggest that effects of approach
speed not only differ among taxa but may also be affected by
other simultaneously operating risk and cost factors.
As predicted by theory, HT decreased as body condition decreased in the lizard P. muralis, presumably because foraging
was more important in individuals in poorer condition (Amo
et al. 2007). However, in the marmot Marmota flaviventris the
3-way interaction between body condition, food presence, and
Cooper • Risk, cost, and refuge
distance from the approaching investigator when the marmot
entered refuge (Rhoades and Blumstein 2007) suggests that
body condition may affect HT in marmots in complex ways.
Body size has a consistent effect on HT, but explanations of it
differ among authors. In all 4 species (an invertebrate, 2 fish,
and a mammal), HT increases as body size increases (Table 3).
Jennions et al. (2003) suggested that larger fiddler crabs hide
longer due to greater risk of predation by birds that preferentially hunt for larger crabs. For the fish, Krause et al. (1998;
Krause, Cheng et al. 2000) suggested that perceived risk does
not vary with body size, but relative weight loss due to food
deprivation while hiding is greater for smaller individuals.
Thus, cost of hiding was greater for smaller fish, leading to
shorter HTs. Blumstein and Pelletier (2005) noted that marmots might have to learn to prolong hiding and considered it
likely that food is especially important to juveniles that must
gain mass quickly to survive hibernation. Effects of body size
on HT may be subject to selective regimes varying among taxa
and are potentially complex due to differences among body
sizes in changes in detectability, escape ability, habitats, and
physiological requirements in prey; changes in predator
suites; and differences in predator hunting methods and preferences. Detailed knowledge for each species may be needed
to determine relative risks and costs of hiding needed to justify predictions about effects of body size on HT. An alternative explanation that applies to all of the above cases is Clark’s
(1994) asset protection principle: Larger individuals may have
higher fitness to protect.
Cost-benefit hypotheses of HT: utility and risk assessment
Due to marked ecological, morphological, and physiological
differences among prey taxa, the importance of various factors
affecting HT varies among taxa. Despite these differences, HT
appears to be universally responsive to variation in costs of
emerging and costs of hiding. This review shows that predictions of cost-benefit approaches for HT have been nearly uniformly verified. Predictions of a break-even model, in which
prey emerge when cost of emerging equals cost of remaining
in refuge (Martı́n and López 1999a), and an optimality model,
in which prey emerge when expected fitness is maximized
(Cooper and Frederick 2007a), are empirically supported.
Critical tests to distinguish between models await measurement of costs and benefits in fitness units. The models currently may be equally useful for ordinal level predictions
about HT for costs of emerging and hiding.
FUNDING
Indiana University–Purdue University Fort Wayne.
I thank D.S. Wilson and the staff of the Southwestern Research Station
for hospitality computational facilities and logistical support. The research was conducted according to approved protocol 00-037-03 of
the Purdue Animal Care and Use Committee. Collection of lizards
was done under Scientific Collecting Permit SP560338 issued by the
Arizona Game and Fish Department. I am grateful to E. Rhoades
and D. Blumstein for generously providing a data set for further examination of the source of interaction between approach speed and HT in
M. flaviventris.
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