Behavioral Ecology Vol. 12 No. 4: 386-389
© 2001 International Society for Behavioral Ecology
Repeated predatory attacks and multiple decisions to come out from a refuge in an alpine lizard
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, 28006 Madrid, Spain
Address correspondence to J. Martín. E-mail: jose.martin{at}mncn.csic.es .
Received 24 March 2000; revised 31 July 2000; accepted 25 August 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Prey often respond to predator presence by increasing their use of refuges. However, because the use of refuges may entail several costs, the decision of when to come out from a refuge should be optimized. In some circumstances, if predators remain waiting outside the refuge and try new attacks or if predator density increases, the prey may suffer successive repeated attacks in a short time. Successive attacks may represent an increase in the risk of predation, but the costs of refuge use also may increase with time spent in the refuge. Thus, prey should make multiple related decisions on when to emerge from the refuge after each new attack. We simulated in the field repeated predatory attacks to the same individuals of the lizard Lacerta monticola and specifically examined the variation in successive times to emergence from a refuge under different thermal conditions (i.e., different costs of refuge use). The results showed that risk of predation but also thermal costs of refuge use affected the emergence decisions. Lizards increased progressively the duration of time spent in the refuge between successive emergence times when the costs of refuge use were lower, but tended to maintain or to decrease the duration of time spent in the refuge between successive emergence times when cost of refuge use increased. Additionally, lizards that entered the refuge with higher body temperatures had overall emergence times of longer duration. Optimization of refuge use and flexibility in the antipredator responses might help lizards to cope with increased predation risk without incurring excessive costs of refuge use.
Key words: antipredator behavior, ectotherms, hiding behavior, lizards, predation risk, refuge use.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Prey often respond to predator presence by increasing their use of refuges (Cooper, 1998
;
Sih, 1986;
Sih et al., 1992). However,
refuge use may have some costs that should be minimised such as, for example,
the loss of time available for foraging
(Dill and Fraser, 1997;
Koivula et al., 1995) or mate
searching (Crowley et al.,
1991; Sih et al.,
1990), and physiological costs, such as hypoxia or hypothermia
(Martín
and López, 1999b;
Wolf and Kramer, 1987). For
this reason, animals should optimize the decision of when to come out from a
refuge after a predator's unsuccessful attack by balancing antipredator
demands with other requirements (Dill and
Fraser, 1997; Sih,
1992,
1997;
Sih et al., 1988). Risks and
costs are balanced in determining when to flee to a refuge
(Ydenberg and Dill, 1986) and
when to emerge from this refuge as well
(Martín
and López, 1999a; Sih,
1992,
1997).
We have previously presented a special case of Ydenberg and Dill's
(1986) model that predicted
how emergence time from the refuge in lizards or other ectotherms should vary
as a function of risk of predation and thermal conditions of the refuge
(Martín
and López, 1999a). In a field
experiment, we showed that the variation in emergence time from a refuge of
the lizard Lacerta monticola supported the predictions of the model
(Martín
and López, 1999a). Thus, time
spent in the refuge decreased when thermal conditions of the refuge were
unfavorable with respect to the thermal conditions outside (i.e.,
physiological costs of refuge use were higher). In this experiment lizards
only had to decide once when to emerge, because we performed only one
simulated attack on each lizard, thus suggesting that the predator had left
the area searching for a new unaware prey after this particular one had
disappeared into a refuge. However, many sit-and-wait predators may remain
waiting for an individual prey outside the refuge and try a new attack.
Alternatively, if predator density increases, the probability of an attack by
a different individual predator also can increase. In these circumstances, a
prey may consider that successive attacks represent an increase in the risk of
predation. Each new attack may indicate that an individual predator persists
in trying to capture that particular prey or that predator density has
increased. Thus, the probability of a predator waiting for the prey outside
the refuge or of a new predator appearing (i.e., probability of a new attack)
will decrease more slowly with time after each successive attack. If predation
risk was the only variable considered by the prey, an optimal response would
require that the prey maximize time spent in the refuge to minimize the risk
of suffering a new attack. Therefore, the successive emergence times should be
longer than the previous one. Thus, when costs of refuge use are low, prey
must tend to increase the time between attempts to emerge from the refuge with
successive attacks.
On the other hand, in many situations the costs of refuge use may increase
with time spent in the refuge. The total costs will be greater as the number
of repeated attacks, and subsequent time spent in the refuge, increase. The
prey should choose to be in the patch (refuge or exterior) with the higher
expected future reproductive success
(McNamara and Houston, 1986);
this depends on prey survival of predation and on refuge conditions for prey
physiological functions. Thus, prey should choose to get out of the refuge
sooner when the costs of refuge use increase, although the risk to fitness of
predation in the exterior might remain high (as indicated by the occurrence of
previous repeated attacks). Thus, when costs of refuge use are high, prey
should tend to maintain or decrease time spent in the refuge with successive
attacks to minimize these costs.
In this article we present the results of a field study to test these predictions in the Iberian rock lizard (Lacerta monticola), a small lizard inhabiting the high altitude mountains of the Iberian peninsula. We simulated repeated predatory attacks to the same individuals and specifically examined the variation in successive times to emergence from a refuge under different thermal conditions (i.e., different costs of refuge use).
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METHODS |
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Species and study site
We performed the study in the Guadarrama Mountains (Madrid Province, central Spain) at an elevation of 1900 m. Granite rock boulders and screes interspersed with shrubs (Cytisus oromediterraneus and Juniperus communis) predominated at the study site, together with meadows of Festuca and other grasses (Martín and Salvador, 1992
). In this area, L. monticola
(snout-to-vent length of adult individuals ranges between 65-90 mm) is active
only from May to September due to limiting environmental temperatures, mating
in May-June and producing a single clutch in July
(Elvira and Vigal, 1985).
Lizards of this species select microhabitats with abundant rocks, where they
escape from predators by hiding under rocks or in rock crevices
(Martín
and Salvador, 1992). However, thermal conditions in the refuges
are often unfavorable and well under the optimal temperature preferred by
lizards (Bauwens et al., 1995;
Martín and
Salvador, 1993).
Procedure
We conducted the study in June 1998. We searched for lizards by walking the
area between 0700 and 1200 h (G.M.T.). Only lizards with complete tails were
included in the analysis because tailless individuals incur a higher predation
risk and may show different antipredator behavior
(Martín
and Salvador, 1993). We approached individual lizards by
simulating a predatory attack by walking directly at the lizard, which
typically made a short flight and hid entirely in the nearest available rock
crevice. To avoid confounding effects that may affect risk perception of
lizards (Burger and Gochfeld,
1993; Cooper, 1997)
the same person wearing the same clothing performed all approaches in a
similar way, while another person recorded the lizard's behavior. When the
lizard hid, we started a stopwatch and retreated to a distance of 5-7 m to
observe from a hidden position with binoculars. We recorded the time that the
lizard spent in the refuge until more than half of the lizard's body emerged
from the refuge (time to emergence). Immediately after a lizard emerged from
the refuge, we approached it, simulating another predatory attack with the
same characteristics, until the lizard hid again. Then, we retreated to a
hidden position to observe and record the second emergence time. We repeated
this procedure with the same individual 10 successive times
(
= 8.9 times, SE = 0.7) or until the lizard
was lost, if it ran away from the refuge. During one trial, total time spent
in the refuge by lizards was on average 145 ± 14 s (range: 58-332 s).
At the end of the trial, we measured with a digital thermometer the
temperature at the point where the lizard was before the attack (air and
substrate temperature), and in the refuge (substrate).
Data analysis
To study the change in times to emergence, we used the difference between
heating rate outside and in the refuge as a measure of thermal cost of refuge
use (see
Martín and
López, 1999a). Potential heating
rates of L. monticola lizards are a function of lizard body mass,
angle of incidence of sun rays on the lizard's body (heliothermic
contribution) and substrate temperature (thigmothermic contribution), as
described in Carrascal et al.
(1992). We assumed that the
angle of incidence of sun rays was a constant outside the refuge because it
may always be maximized through behavioral adjustments of basking postures
(Martín et
al., 1995), while this value was equal to zero in the shaded
refuge. Body mass was also constant for a given individual. Thus, in our study
the only variable for a given individual was the difference between external
and refuge substrate temperatures (temperature differential).
To study the change in response over a trial (i.e., changes in times to
emergence), we used Pearson's product-moment correlation coefficient,
r, to test the null hypothesis of r > 0 (times to
emergence increase; i.e., lizards consider only the increase in predation
risk) against the alternative hypothesis r 
0 (times to emergence
decrease or maintain the same level; i.e., lizards consider the costs of
refuge use) (Sun and
Müller-Schwarze, 1998). The
correlation coefficient, r, and the slope, b, of the
estimated regression line measured the overall trend of response during each
trial. Time to emergence data were log-transformed to ensure normality before
calculating r and b. To analyze the relationships between
changes in times to emergence and thermal costs of refuge use, we used Pearson
linear regression between the measures of change within a trial (r or
b) and the difference between external and refuge substrate
temperatures (Sokal and Rohlf,
1995). We also calculated the average duration of all the
successive emergence times along the trial, as a measure of the trade-off
between costs of refuge use and predation risk. The average duration of times
to emergence, the temperature differential and lizards' initial body
temperature were log-transformed to ensure normality.
Given the large size of the area surveyed (more than 5 km2), the high lizard density, and because we avoided walking routes taken previously, the probability of repeated sampling of the same individual was very low. We therefore treat all measurements as independent.
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RESULTS |
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The coefficients of regression (r) of successive times to emergence in a trial (which measured the overall trend of response during each trial) decreased when the difference between external substrate temperature and refuge temperature increased (r = -.68, F = 21.85, df = 1,31, p =.0001) (Figure 1). Similarly, the slopes (b) of the regression lines, calculated for each trial, also decreased when the temperature differential increased (r = -.49, F = 9.48, df = 1,31, p =.004) (Figure 1). Thus, lizards increased progressively the duration of the successive times to emergence (r and b > 0) when the costs of refuge use were lower, but tended to maintain or to decrease (r and b
0) the
duration of successive times to emergence when cost of refuge use
increased.
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In contrast, the average duration of all times to emergence along a trial did not significantly change with the temperature differential (r = -.13, F = 0.15, df = 1,31, p =.46). However, the average duration of times to emergence was probably dependent on a lizard's initial body temperature, because it was significantly affected by the external temperature (r =.50, F = 9.78, df = 1,31, p =.004) (Figure 2). Thus, lizards that entered the refuge with higher body temperatures had overall times to emergence of longer duration.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The results of this experiment showed that risk of predation but also thermal costs of refuge use affected the duration of successive times to emergence from the refuge in L. monticola. Initially, an increase in the frequency of predatory attacks was probably interpreted as an increase in the probability of a new attack (i.e., diminution of predation risk with time is slower). Thus, when costs of refuge use are low, lizards tended to increase the duration of successive times to emergence to compensate for the increase in predation risk. This result agrees with the general tendency of many animals, including lizards, which modify their microhabitat or refuge use according to the estimated levels of predation risk (Lima and Dill, 1990
;
Martín and Salvador,
1992,
1993;
Sih et al., 1992). In another
experiment, the skink Eumeces laticeps also remained in refuges
longer after the second of two successive similar approaches than after the
first (Cooper, 1998). These
data may indicate that lizards perceived a higher predation risk due to
persistence by an individual predator, although individual recognition of the
predator may not be needed if the assessment was just based on attack rate
(Cooper, 1998).
However, use of refuges by L. monticola may entail more costs than
for lowland species because montane lizards are subjected to variable
radiation levels and low environmental temperatures that constrain their
activity times to a larger extent than at lower altitudes
(Sinervo and Adolph, 1994). It
is not surprising that L. monticola optimize their refuge use to
minimize the time spent at unfavorable temperatures and the waste of time that
could be devoted to other activities
(Martín
and López, 1999a). Thus, when the
costs of refuge use increased, lizards tended to maintain or even to decrease
the duration of successive times to emergence, in spite of the increase in
predation risk. Alternatively, a decrease between successive emergence times
might also be compatible with lizards habituating to the predator and ceasing
to consider it a threat. However, this possibility could be dismissed because
habituation is unlikely to be correlated with temperature differences.
Occasionally, when thermal costs were excessively high, we observed that
some individuals that emerge from the refuge were reluctant to enter again
with a short run after a successive attack. In contrast, these lizards
performed an alternative escape tactic, running for longer to other refuges
less safe or that were placed further (e.g., broom bushes) but where thermal
costs were lower. Thus, lizards may assume a higher predation risk by being
exposed for longer to a predator pursuit, but could decrease the costs
resulting from refuge use. Similarly, expected long-term fitness costs of
refuges also affected escape decisions of L. monticola, which had
longer approach distances when the external heating rate and the refuge
cooling rate were lower (i.e., when thermal costs were lower)
(Martín
and López, 2000).
The results also suggested that when lizards' initial body temperature was
high, they could afford to increase time spent in the refuge. One of the costs
of refuge use was probably the decrease of lizards' body temperature with
time. Body temperature influences many aspects of lizard behavior including
burst speed (Bauwens et al.,
1995). Lizards with low body temperatures are more vulnerable to
predation due to lower escape performance
(Christian and Tracy, 1981). It
is likely that, independently of other time costs, there could be a critical
low value of body temperature when lizards should switch their antipredator
strategy and emerge from the refuge to regain optimal body temperature.
Because the probability of a new attack is high, lizards with excessively low
body temperatures may be unable to run effectively to the refuge in case of a
new attack. Thus, it would be advantageous to emerge when locomotor
performance is still high because, although they might expose themselves to a
new attack, the predator could be eluded easily with a short run to the
refuge. In contrast, emerging with low body temperature and associated low
performance would require some time spent in basking before regaining their
optimal body temperature and sprint speed appropriate to escape. In accordance
with this prediction, and similarly to the lizard P. muralis
(Martín
and López, 1999b), L.
monticola that entered the refuge with higher initial body temperatures
had overall times to emergence of longer duration. If this constraint exists,
it might also explain why under unfavorable refuge thermal conditions the
successive times to emergence tended to decrease. As body temperature decrease
continuously in a cool refuge, the time to reach the critical temperature will
be shorter after each successive attack, forcing the lizard to emerge sooner.
Other studies have shown that recovering at a cool temperature severely
retarded the ability of the lizard Dipsosaurus dorsalis to repeat
both exhaustive and sprinting exercises
(Wagner and Gleeson, 1997).
Thus, it would be advantageous to emerge as soon as possible from a cool
refuge.
The observed variation within successive emergence times might be also
interpreted as a method to assess predation risk levels in the exterior more
effectively. The decision to recover the normal activity will depend on the
information on the presence of the predator, and many times this can only be
known after emergence. Sampling for predator persistence at variable intervals
of time may increase the quality of prey information, helping to decide the
optimal antipredator strategy. Dynamic models have suggested that animals will
show tolerance to imperfect information, but that the extent of this tolerance
may change from one situation to the next, and that the rules of thumb should
be flexible to local ecological conditions
(Koops and Abrahams, 1998). In
our experiment, the variation of successive times to emergence may be
interpreted as a way to prevent the predator from being able to predict when
the lizard would emerge again. This may represent a mixed evolutionarily
stable strategy to a hiding-waiting game between prey and predators
(Johansson and Englund,
1995).
We conclude that an increase in predation risk may force animals to use antipredator behaviors having increased associated costs (i.e., increasing time spent in the refuge). However, optimization of refuge use and flexibility in the antipredator responses (e.g., variability in the times to emergence) might help lizards to cope with changes in predation pressure without incurring excessive physiological costs.
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ACKNOWLEDGEMENTS |
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We thank two anonymous reviewers for helpful comments, and "El Ventorrillo" MNCN Field Station for use of their facilities. Financial support was provided by the DGESIC project PB-98-0505 and a CSIC contract to P.L.
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