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Behav Ecol Sociobiol (2003) 54:505–510
DOI 10.1007/s00265-003-0659-3
ORIGINAL ARTICLE
J. Martn · P. Lpez · W. E. Cooper
Loss of mating opportunities influences refuge use
in the Iberian rock lizard,
Lacerta monticola
Received: 6 April 2002 / Revised: 6 May 2003 / Accepted: 12 June 2003 / Published online: 22 July 2003
Springer-Verlag 2003
Abstract Because time spent in refuge may be costly if
prey lose opportunities to forage, fight, or mate, prey
allow predators to approach closer before beginning to
flee when opportunity costs are high. Because the same
opportunity costs may apply to refuge use as to escape,
prey should make similar trade-offs between risk of
emerging and cost of remaining in refuge. In the Iberian
rock lizard, Lacerta monticola, we studied the effects of
sex, reproductive season, speed of predator approach, and
potential loss of mating opportunities on time spent in
refuge following simulated predatory attacks. Lizards of
both sexes adjusted refuge use to the level of risk by
spending more time in refuge when approached rapidly
than slowly. Females remained in refuge for equal times
in the mating and postreproductive seasons, but males
emerged sooner during the mating season, suggesting
adjustment to a cost of lost opportunity to search for
mates during the mating season. When a tethered female
was nearby, males emerged from refuge earlier than if no
female was present, indicating a trade-off between risk
and mating opportunity. Approach speed affected emer-
gence time when females were absent, but not when a
female was present. Approach speed did not affect the
probability that, after emerging, a male would return to
court the female. For males that courted females intensely
(bit them) before entering refuge, approach speed did not
affect latency to emerge, but males that courted less
intensely emerged sooner if approached slowly than
rapidly. These findings show that males adjust the length
of time spent in refuge to both risk of predation and
reproductive cost of refuge use.
Keywords Refuge use · Lizards · Costs of reproduction ·
Antipredatory behavior · Mating opportunities
Introduction
An increasing number of studies are reporting that
predation risk is a major cost of reproduction (see review
in Magnhagen 1991). Reproductive activities per se may
expose both sexes to increased risk of predation, and thus
many animals compensate by decreasing mating activities
(Candolin 1997; Koga et al. 1998; Krupa and Sih 1998) or
by modifying some aspects of behavior (e.g. Cooper et al.
1990; Lima and Dill 1990). However, limited mating
opportunities may force animals to increase risk-taking
behaviors (Hazlett and Rittschof 2000). For instance,
animals may delay escape decisions (i.e. increasing
exposure to predation) when the costs of losing oppor-
tunities for mating or defending a reproductive territory
increase (Cooper 1999; Daz-Uriarte 1999; Martn and
Lpez 1999a). The optimal antipredatory behavioral
decision may depend on the individual’s current repro-
ductive prospects (asset-protection principle, Clark 1994).
Thus, animals may be less responsive to predation risk
during the reproductive season than during the non-
reproductive season. For example, some prey fish species
may largely ignore predators during the reproductive
period (Helfman 1986).
Prey often increase refuge use to cope with predatory
attacks (Sih 1986; Sih et al. 1992; Cooper 1998).
However, refuge use may be costly in terms of the loss
of time available for foraging (Koivula et al. 1995; Dill
and Fraser 1997) or mate searching (Sih et al. 1990;
Crowley et al. 1991), or because of physiological costs
(Wolf and Kramer 1987; Martn and Lpez 1999b). For
this reason, animals should optimize the decision of when
to emerge from a refuge after a predator’s unsuccessful
attack by balancing antipredator demands with other
Communicated by A. Mathis
J. Martn (
)
) · P. Lpez
Departamento de Ecologa Evolutiva,
Museo Nacional de Ciencias Naturales,
CSIC, Jos Gutirrez Abascal 2, 28006 Madrid, Spain
e-mail: Jose.Martin@mncn.csic.es
Fax: +34-91-5645078
W. E. Cooper Jr.
Department of Biology,
Indiana University-Purdue University Fort Wayne,
Fort Wayne, IN 46805, USA
requirements (Sih et al. 1988; Sih 1992, 1997; Dill and
Fraser 1997). Flexibility in the antipredatory responses
might help animals to cope with predation risk without
incurring excessive costs of refuge use (Sih 1992, 1997;
Martn and Lpez 1999c, 2001). Several costs (e.g., loss
of mating or feeding opportunities) and benefits (i.e.,
diminution of predation-risk levels) should be balanced
when deciding optimal emergence times from refuges.
These multiple factors may naturally vary together and,
thus, animals should be able to assess the variations in one
or both of these factors simultaneously. Many animals are
able to modify their antipredatory behavior according to
the estimated levels of predation risk (Lima and Dill
1990; Sih et al. 1992), which prey may assess sometimes
from the predator’s behavior (Burger and Gochfeld 1990,
1993; Martn and Lpez 1996; Cooper 1997a, 1997b).
Emergence times from a refuge may depend on the
characteristics (i.e., risk level) of the previous attack of
the predator (Cooper 1998; Martn and Lpez 1999c).
Different levels of risk and different benefits to be gained
after emerging may, thus, lead to different optimal
solutions of refuge use.
Polygyny is widespread in lizards, although the range
of number of females per male is substantial (Stamps
1983). For copulation, a male must find a female within
her home range and court her there (Stamps 1983). Thus,
to access more than one female, males should increase
movements during the mating season. Repeated searches
of the home range increase the encounter rate of males
with prospective mates (McCloskey et al. 1987). How-
ever, there may be a trade-off between mating and
antipredator requirements if increased movements attract
predators (Magnhagen 1991). Also, time spent in the
refuge by males after an unsuccessful predatory attack
may reduce the time available for searching for females,
and thus decrease their opportunities for reproduction.
Thus, we hypothesized that male lizards should risk more
(i.e., have shorter emergence times) in the mating season
and when a receptive female is actually present. However,
the antipredatory responses under different expected
opportunities of mating should also depend on the level
of predation risk. Because the reproductive success of
females does not depend on number of matings, cost of
refuge use is not expected to vary as greatly for females as
for males between the mating and postreproductive
seasons. Thus, statistical interaction is expected between
sex and season.
In this paper, we present the results of a field study to
test these predictions in the Iberian rock lizard (Lacerta
monticola), a small lizard inhabiting high-altitude moun-
tains of the Iberian peninsula. At high altitude, cool
temperatures limit activity of lizards (Carrascal et al.
1992), making use of refuges costly (Martn and Lpez
2000). Lizards are active from May to October, but the
daily period with thermal conditions suitable for activity
is often restricted by severe climatology. Mating occurs
during a limited period of about 2 weeks in May/June, and
females produce a single clutch in July (Elvira and Vigal
1985). Males are polygynous: the number of females is
approximately double that of males (Prez-Mellado et al.
1987). Males gain access to several females by increasing
their movements and home-range size (Martn and
Salvador 1997; Aragn et al. 2001). With respect to their
antipredator behavior, approach distances and emergence
times from refuges may vary as a function of predation-
risk level and costs of refuge use (Martn and Lpez
1999c, 2000, 2001).
We conducted two experiments to test whether poten-
tial mating opportunities influenced the time lizards spent
in refuges. The first experiment examines whether there
are differences between the sexes in the responses to
different levels of predation risk, and whether these
responses change from the mating to the postreproductive
season. In a second experiment, conducted during the
mating season, we introduced tethered females to males,
and then simulated a predatory attack by approaching
lizards directly at one of two different approach speeds.
We compared emergence times of these males to control
males that were not exposed to females.
Methods
Study area and general methods
We performed the study in the Guadarrama Mountains (Madrid
Prov., central Spain) at an elevation of 1,900 m. Granite rock
boulders and screes interspersed with shrubs (Cytisus oromediter-
raneus and Juniperus communis) predominated at the study site,
together with meadows of Festuca and other grasses (Martn and
Salvador 1992). We searched for lizards by walking the area
between 0700 and 1200 hours G.M.T.). Only adult lizards (approx.
snout-to-vent length, SVL>75 mm) with complete tails were used
in the experiments. Before the trials, we noted their sex, which was
easily identifiable at a distance by dorsal coloration (green males vs
brown females) and morphological features (i.e., large head-size
proportions of males). To ensure that each lizard was tested only
once, we moved through a given portion of the study site once on
1 day and then moved to a new location for further observations on
another day. Also, observations from the two seasons were made in
sectors within the same area having identical characteristics, but
separated by 1.5 km. Given the large size of the area surveyed
(more than 5 km
2
) and the high lizard density, the probability of
repeated sampling of the same individual was very low. We
therefore treated all measurements as independent.
Effects of sex, predator speed, and season on emergence times
We conducted this experiment during May (mating season) and
July (postreproductive season). When we detected a lizard, we
approached it directly at one of two different approach speeds: slow
(ca. 45 m/min) or fast (ca. 140 m/min). We predicted that rapid
approach should be considered by lizards as a higher risk of
predation (Cooper 1998). To avoid confounding effects that may
affect risk perception of lizards (Burger and Gochfeld 1993; Cooper
1997b), the same person wearing the same clothing performed all
approaches.
Lizards typically made a short flight to the nearest available
refuge (under a rock or into a rock crevice) and hid entirely from
the observer. When a 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 (emergence time). We tested a total of 80 lizards, 10 males
and 10 females in each treatment (slow vs fast) during the mating
506
season, and another 10 males and 10 females in each treatment
during the postreproductive season.
Effects of female presence and predator approach speed
on emergence times
We conducted this experiment during May/June 2001, which
coincided with the mating season of lizards in this population
(Aragn et al. 2001). Each day we captured by noosing two to three
adult females (SVL ranged between 75 and 82 mm). We selected
females that had not mated yet, as indicated by characteristic
mating scars on the belly (personal observation), because after
mating females may be unreceptive to males. Each female
participated in a maximum of five trials, and was kept in a small
terrarium between trials. We released females at the same capture
sites at the end of the trials after a maximum of 4 h.
When we detected an adult male lizard, one experimenter slowly
approached it and stopped at a distance of 2 m. Usually, lizards
permitted such close approach at slow speed without attempting to
escape. We slowly moved either a tethered female or a small piece
of wood having the approximate size and shape of a female to a
position 0.5 m from the male. The wood served as a control for the
effects of the experimental disturbance. The female or wood was
tied to a 1-m rod by a 0.3-m string. Males typically approached the
female and started to court her, or remained close to the introduced
wood. During courtship displays, the male approached the female
slowly and began to tongue-flick the body or tail or the surrounding
substrate. He next gripped and shook the female’s tail with a gentle
bite, and then attempted mounting. The experimenter waited
immobile after courtship began or a similar period of time (about
20 s) in the control treatment. Thereafter, another experimenter
chased the lizard as above, simulating a predatory attack directly at
one of two different approach speeds (slow vs fast, see above),
forcing the lizard to hide in a rock crevice, and then retreated. The
order of presentation of the different treatments was counterbal-
anced. We tested 20 different males in each treatment.
Trials were aborted if lizards showed signs of disturbance and
escaped before being chased due to the observer’s presence.
Lizards typically made a short flight to the nearest available refuge
and hid entirely from the observer. When the lizard hid, we started
a stopwatch, and the experimenter that remained immobile close to
the refuge slowly moved either the tethered female or the wood
within 15 cm of the refuge. We recorded the time until more than
half of the male’s body emerged from the refuge (emergence time)
(Martn and Lpez 1999c). In the female treatments, we also
recorded whether the male returned to court the introduced female
again, and the time elapsed since emergence to the start of the new
courtship. We also noted whether the male had bitten the female
during the first courtship approach.
Data analyses
Because temperature can affect emergence times of lizards (Martn
and Lpez 1999c), immediately after a lizard emerged from the
refuge and resumed its activity, we used a digital thermometer to
measure the substrate temperatures at the point where the lizard
was before the attack and in the refuge. Thermal costs of refuge use
were estimated from the difference between substrate temperature
outside and in the refuge (see Martn and Lpez 1999c). Also,
potential body temperatures can be estimated from substrate
temperatures according to the relationship described by Martn
and Salvador (1993). These thermal costs and potential body
temperatures did not differ significantly among treatments in any of
the experiments (ANOVAs, P>0.45 in all cases), and thus could not
have influenced the results of these experiments.
In the first experiment, we used three-way ANOVA to analyze
differences in emergence times between approach speed, sex, and
seasons. We included the interactions in the model to analyze how
the responses of males and females may vary with the season, and
whether the responses to different approach speeds vary between
sexes or seasons. In the second experiment, we used two-way
ANOVAs to assess differences in emergence time among treatments.
We included the interaction between female presence and speed of
approach to examine how different levels of predation risk might
influence the males’ response to the female presence. Data were log-
transformed to achieve normality. Tests of homogeneity of variances
(Levene’s test) showed that, in all cases, variances were not
significantly heterogeneous after transformation (Sokal and Rohlf
1995). Differences between pairs of treatments were assessed a
posteriori using Tukey’s honestly significant difference (HSD) tests.
Results
Effects of sex, predator speed, and season
on emergence times
After a predatory attack, lizards emerged significantly
earlier when the approach was made at slow speed than
when it was made at fast speed (three-way ANOVA, speed
effect: F
1,72
=7.87, P=0.006), but the sexes did not differ
significantly (sex effect: F
1,72
=0.04, P=0.95), and the
difference between the mating and the postreproductive
seasons was also not significant (season effect: F
1,72
=3.78,
P=0.056) (Fig. 1). However, the interaction between sex
and season was significant (sexseason effect: F
1,72
=4.31,
P=0.04), with males having shorter emergence times in the
mating than in the postreproductive season (Tukey’s HSD
tests, P=0.029), whereas females did not differ in emer-
gence times between seasons (P=0.99). All other interac-
tions were non-significant (seasonspeed: F
1,72
=0.47,
P=0.49; sexspeed: F
1,72
=0.10, P=0.75; speedsexsea-
son: F
1,72
=2.15, P=0.15).
Effects of female presence and predator
approach speed on emergence times
After a predatory attack, males emerged significantly
earlier from the refuge when a female was present than in
the control situation (two-way ANOVA, female effect:
F
1,76
=85.55, P<0.0001) (Fig. 2), and emerged significant-
Fig. 1 Emergence times (X
¯
€1 SE) from a refuge of male (filled
circles) and female (unfilled circles) Lacerta monticola lizards after
being approached directly by an experimenter at one of two
different approach speeds (slow vs fast) in the mating or the
postreproductive seasons
507
ly earlier when the approach was made at slow speed than
when it was at fast speed (speed effect: F
1,76
=19.67,
P<0.0001). The interaction between female presence and
predator speed was not significant (F
1,76
=2.71, P=0.10).
However, post-hoc tests indicated that, in the control
situation, males emerged significantly earlier when the
speed was slow (Tukey’s HSD test, P=0.0004), but that
emergence times did not differ significantly between
approach speeds when a female was present (P=0.21).
The approach speed did not significantly affect the
propensity of the male to return and court the female after
the predatory attack (16 vs 10 males returned to court
after being approached rapidly or slowly, respectively; 2-
tailed binomial test P=0.33). Emergence times did not
differ significantly between males that returned to court
(X
¯
€SE=10.0€1.4 s, n=26) and males that did not return
(8.7+1.6 s, n=14) (ANOVA: F
1,38
=0.16, P=0.69). When
males returned to court the female, latency to resume
courtship after emerging from the refuge did not differ
significantly between predator approach speeds (fast:
X
¯
€SE=4.7+0.8 s; slow: 3.6+1.0 s; ANOVA: F
1,24
=0.21,
P=0.65).
When a male bit a female during courtship, it might be
considered that the interest of this male in the female was
greater than when a male licked the female, but did not
attempt to mount her. All males that had bitten the female
returned to court her after the attack. However, emer-
gence times did not differ significantly between males
that bit and those that did not bite the female (two-way
ANOVA, bite effect: F
1,36
=0.26, P=0.31) or between
approach speeds (speed effect: F
1,36
=1.09, P=0.30), and
the interaction was not significant (F
1,36
=1.03, P=0.30).
Nevertheless, in a separate analysis, emergence times did
not differ significantly between approach speeds for
males that bit the female (fast: X
¯
€SE=7.8+1.7 s; slow:
7.5+1.4 s; ANOVA: F
1,7
=0.001, P=0.98), but for males
that did not bite females, emergence times were signif-
icantly longer for fast than slow approaches (fast:
X
¯
€SE=12.9+2.2 s; slow: 7.5+1.4 s; ANOVA: F
1,29
=
4.22, P<0.05).
Discussion
The different levels of predation risk posed by a predator
approaching at different speeds strongly affected latency
to emerge from refuge. Rapid approach by a predator is an
important indicator of immediate threat of predation to
which prey in many species respond by increasing both
the flight-initiation distance (e.g., Dill 1974; Martn and
Lpez 1996; Cooper 1997a; but see Bonenfant and
Kramer 1996) and latency to emerge from refuge (Cooper
1998; Martn and Lpez 1999c).
Many animals, such as some fishes (Endler 1987;
Candolin 1997), frogs (Ryan et al. 1982), crabs (Koga et
al. 1998), or aquatic insects (Sih et al. 1990), may reduce
mating activity under predation risk. However, when
there is a trade-off between mating opportunities and
predator avoidance, the degree of risk taking should be
related to the probability of future mating opportunities
(Magnhagen 1991; Clark 1994). Thus, for example,
young Gobius niger fishes stopped spawning under
predation risk, whereas older individuals readily spawned
in a similar situation (Magnhagen 1990). Similarly, in L.
monticola, where the mating period is very short, sex and
season also affected decisions about refuge use, as
indicated by the significant interaction term. During the
mating season, males had shorter emergence times than in
the postreproductive season. Male L. monticola also have
greater general activity levels during the mating season
and these seasonal differences cannot be explained by
thermal constraints or changes in microhabitat use
(Aragn et al. 2001). Thus, when mating opportunities
are high, males seem to be less sensitive to predation risk,
at least in a situation where the predator has disappeared
after an unsuccessful attack. Nevertheless, it may be
expected that an increase in risk may force prey to
increase emergence times. Thus, in the second experiment
during the mating season, when we increased risk by
remaining close to the refuge, emergence times were
longer and were affected by approach speed in the control
treatment, but not in the female treatment. Therefore,
variations in emergence times seem to reflect different
balances between the costs of losing mating opportunities
and the benefit of a diminution of predation risk with
time.
The absence of any effect of season on refuge use of
females may be explained in part by the greater repro-
ductive investment of females (Clark 1994) and by the
lack of a relationship between reproductive success and
number of matings. Whereas males can increase the
number of eggs fertilized by mating with multiple
females, females may fertilize all their eggs by mating
once. Thus, females should risk less than males. Also,
during the mating season, female L. monticola remain
relatively stationary, but males must search for females
(Martn and Salvador 1997; Aragn et al. 2001). Thus,
females do not lose reproductive opportunities by in-
creasing refuge use. Nevertheless, it might be expected
that gravid females later in the year have greater latency
to emerge than males or nongravid females because their
Fig. 2 Emergence times (X
¯
€ 1 SE) from a refuge of male Lacerta
monticola lizards in presence or absence (control) of a tethered
female after being approached directly by an experimenter at one of
two different approach speeds (slow vs fast) in the mating season
508
risk of predation is greater in many species due to
decreased sprint speed, which impairs their ability to
escape (Shine 1980; Cooper et al. 1990; Magnhagen
1991). Gravid lizards are known to modify other aspects
of antipredatory behavior and may be predicted to spend
more time in refuge unless the increased risk is
outweighed by decreases in body temperature while in
refuge (Martn and Lpez 1999b, 1999c) at a time when
basking may be important for development of offspring.
Thus, the concurrence of different ecological pressures
may lead females to have similar optimal emergence
times in the different phases of their reproductive cycle.
When a tethered female was presented, males had even
shorter emergence times, and these did not differ between
approach speeds. When a female is nearby, staying in the
refuge may result in losing opportunities to mate. A similar
situation was observed in mate-guarding males of the skink
Eumeces laticeps (Cooper 1997a, 1999) and the lacertid
lizard Psammodromus algirus (Martn and Lpez 1999a),
which allowed closer approach than males found alone,
before escaping from potential predators. Because costs of
fleeing and refuge use increase for a male that must leave
his mate to escape, an optimal decision requires that the
approach distance and emergence time decrease even if
predation risk increases (Ydenberg and Dill 1986; Martn
and Lpez 1999a). A male leaving a female not only loses
mating opportunities, but also risks sneaked copulations by
subordinate males if they are not able to relocate their
mates immediately after the predatory attack. Risk of loss
of copulations to rivals may be high in dense populations
such as the one we studied (Martn and Salvador 1997;
Aragn et al. 2001). Risk of losing mating opportunities
due to inability to relocate the female may be especially
great for transient females and unfamiliar females (Cooper
1985), in which case our results may indicate maximum
effects of female presence.
Return by males to court tethered females despite the
proximity of the predator indicates the willingness of males
to take risks to obtain mating opportunities. The predator’s
approach speed influenced neither a male’s decision to
return to court, nor the latency to resume courtship after
emergence. Furthermore, in males that had already attempt-
ed mounting (i.e., those that had bitten the female), the value
of the female was probably assessed as greater, and
emergence times decreased regardless of approach speed.
Taken together, the results of both experiments suggest
that males adjust emergence times simultaneously to the
degree of predation risk and the cost of lost mating
opportunities. Therefore, refuge use in the lizard L.
monticola reflects a trade-off between survival and
reproduction.
Acknowledgements We thank two anonymous reviewers for
constructive and helpful comments, and “El Ventorrillo” MNCN
Field Station for use of their facilities. Financial support was
provided to J.M. and P.L. by the MCYT project BOS 2002-
00547and to W.E.C. by an International Travel Grant from Purdue
University. W.E.C. is grateful for logistical help by Valentn Prez-
Mellado. The experiments were performed under license from the
Agencia del Medio Ambiente de la Comunidad de Madrid (Spain).
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