Behavioral Ecology Vol. 10 No. 4: 452-461
© 1999 International Society for Behavioral Ecology
Male mating strategies under predation risk: do females call the shots?
Behavioural Ecology Research Group, Department of Biological Sciences, Simon Fraser University, Burnaby, BC V5A 1S6, Canada
Address correspondence to A. V. Hedrick, who is now at the Department of Neurobiology, Physiology and Behavior, University of California-Davis, Davis, CA 95616, USA. E-mail: avhedrick{at}ucdavis.edu
Received 16 April 1998; accepted 9 January 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Many authors have reported that, under elevated risk of predation, male guppies (Poecilia reticulata) alter their behavior from courtship to forced copulation (gonopodial thrusts not preceded by sigmoid displays). This shift is presumed to benefit the brightly colored male, whose intense courting activity might otherwise increase his risk of detection and attack by predators. However, there is some evidence that females engaged in reproductive activity with males may be even more vulnerable to predators than the males themselves, which suggests an alternative hypothesis: females in high-risk situations are less receptive to male courtship, and this leads males to change their behavior. We tested this hypothesis by providing either males and females separately, or both sexes concurrently, with information about elevated predation risk from a cichlid (Crenicichla sp.). We found that when only females were provided with information about increased risk, males performed fewer courtship displays and fewer thrusts. They did not perform more forced copulations in any treatment group. Nonetheless, our results suggest that the female's perception of predation risk can be at least as important as the male's in changing male mating behavior.
Key words: courtship, guppies, mating behavior, Poecilia reticulata, predation.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Brightly colored males occur in many species of animals, where their conspicuous coloration can be advantageous in attracting potential mates (Andersson, 1994
). Although
bright colors may entice females of the same species, they can also attract
predators, thereby elevating the male's risk of predation
(Lima and Dill, 1990;
Magnhagen, 1991). Female
choice for bright males and an enhanced risk of predation for bright males
have both been well documented (e.g.,
Endler, 1980;
Hill, 1990;
Houde, 1987;
Kodric-Brown, 1985;
Moodie, 1972;
Semler, 1971).
Less attention has been focused on the risk of predation for females that
are attracted to bright males. Inconspicuous females mating with colorful
males may also be vulnerable, because predators that are attracted to males
can detect females once they approach the pair. Few studies have investigated
the costs for females of associating with conspicuous males in order to mate
(but see Gibson and Bachman,
1992; Pocklington and Dill,
1995). Nonetheless, evidence suggests that females are sensitive
to predation risk and change their mating decisions with levels of risk. In
the cricket Gryllus integer, for example, females choose males with
less preferred calls in safe locations rather than males with more preferred
calls in dangerous locations (Hedrick and
Dill, 1993). Female sand gobies (Pomatoschistus minutus)
also become less selective in mate choice when predation risk increases
(Forsgren, 1992). In the guppy
(Poecilia reticulata), a small, Trinidadian fish, females under
predation risk associate with less colorful males when given a choice between
these and the more conspicuous males they would otherwise prefer
(Godin and Briggs, 1996;
Gong and Gibson, 1996).
Male guppies also respond to predation risk by altering their mating behavior (see below), making guppies a good species in which to compare the relative sensitivity of males versus females to predation risk during mating activities. Here, we examine the differential effects of male versus female exposure to predation risk on courtship and mating behavior of males within pairs of guppies.
Study species
Male guppies bear a series of orange, yellow, iridescent blue, and black
spots, whereas females are drab (Endler,
1987). Males offer no resources other than sperm to their mates.
Females are receptive only as virgins and for a short period following
parturition. Because few females are receptive at any one time
(Kodric-Brown, 1993),
receptive females often can choose among several males vying for their
attention (Kodric-Brown,
1985). Before mating, males commonly perform courtship displays
(sigmoid displays) in which they curve their bodies into an arc or S-shape and
quiver in front of the female. Females can either accept or reject males
following these displays (Luyten and
Liley, 1985). Fertilization is internal via the male's gonopodium,
which he inserts into the female's genital pore using gonopodial thrusts
(Luyten and Liley, 1985).
Although female mate choice is based on multiple criteria
(Kodric-Brown, 1993), many
studies have shown that females generally prefer more colorful males as mates
(e.g., Houde, 1987;
Kodric-Brown, 1985;
Long and Houde, 1989). Thus,
female choice presumably selects for brighter male colors in this species.
However, bright male coloration in guppies also increases predation risk.
Males from streams with high levels of predation are less colorful than males
from streams with low predation (Endler,
1995), and selection experiments have shown that high predation
selects for cryptically colored males, whereas female choice (and low
predation) selects for brighter males
(Endler, 1980). Predation
affects many other life-history characteristics in the guppy, including clutch
size (reviewed in Endler,
1995). Additionally, male coloration (specifically, orange spots)
and female preferences for orange males are often genetically correlated
(Houde and Endler, 1990;
Stoner and Breden, 1988).
Therefore, male coloration in guppies is thought to result from a balance
between female choice favoring brighter colors, versus predation selecting for
less conspicuous colors (Endler,
1980; Houde,
1987).
Predation risk affects male mating behavior as well as male coloration.
Male guppies under predation risk often switch from their normal courtship
sequence, which begins with the conspicuous sigmoid display, to a
"sneaky" mating tactic, in which they perform gonopodial thrusts
without displaying first (Endler,
1987; Godin, 1995;
Luyten and Liley, 1985;
Magurran and Seghers, 1990;
Reynolds et al., 1993).
Although this strategy entails a lower probability of successful insemination
(Liley, 1966), it is probably
less conspicuous to predators than sigmoid displays
(Endler, 1987). Therefore, the
behavioral shift has been interpreted as an adaptive response by the male to
his own perception of danger (Endler,
1987; Magurran and Seghers,
1990).
Males also switch to the alternative, sneaky strategy, however, when
females are unreceptive to sigmoid displays
(Luyten and Liley, 1985).
Moreover, females are also exposed to predation risk during mating activities
and sometimes respond to risk by moving away from males
(Godin and Briggs, 1996;
Gong and Gibson, 1996). This
suggests an alternative interpretation for the switch in male behavior:
perhaps males adopt the sneaky strategy because females change their behavior
when they perceive predation risk, becoming less receptive to male
courtship.
Female guppies may be even more vulnerable to predation than males. Natural
guppy predators are differentially attracted to females
(Pocklington and Dill, 1995),
and females are generally larger than males, making them especially profitable
prey items (Pocklington and Dill,
1995). Females must survive to parturition to achieve reproductive
success after mating, whereas mated males do not. Furthermore, females seem
particularly sensitive to predation risk. Females exposed to predators are
more likely than males to school (Magurran
and Nowak, 1991) and to "inspect" the predator by
approaching it closely. By inspecting, they often subject themselves to forced
copulations by males (Magurran and Nowak,
1991). Inspection may also provide females with additional
information about predation risk
(Magurran, 1990), which could
affect their mating behavior. Females exposed to predation risk spend less
time near males and are less attracted to colorful males, instead associating
with inconspicuous males when given a choice
(Godin and Briggs, 1996;
Gong and Gibson, 1996). These
observations suggest that females may become less receptive to male courtship
when they perceive that predators are present nearby. If so, males may respond
by trying to sneak a mating. Alternatively, males may respond by depressing
their own mating activity. Depression of mating activity occurs as a response
to predation risk in many species
(Magnhagen, 1991).
Hypothesis and predictions
We hypothesized that changes in male mating behavior with predation risk
are due more to the female's perception of predation risk (and her response to
it) than the male's. This hypothesis explicitly addresses changes in male
behavior, and therefore we focused on male behavior here. Our study examined
male courtship and mating behavior in guppy pairs when (1) the male alone sees
a predator, (2) the female alone sees a predator, (3) both sexes see a
predator, and (4) neither sex sees a predator, in a short period immediately
before being allowed access to one another. Because predator inspection
apparently affected our results, we also examined whether and how predator
inspection influences the outcome of mating trials. Predator inspection is
common in guppies, particularly females
(Magurran and Nowak, 1991),
may be performed by inherently "bold" individuals
(Wilson et al., 1994), and is
thought to provide inspectors with additional information on predation risk
which affects their subsequent behavior
(Magurran, 1990).
Specifically, we tested the predictions that:
- When both sexes are exposed to predation risk, mating activity of males
will change to less conspicuous strategies relative to the control situation.
Potentially, thrusts will become relatively more common and sigmoid displays
relatively less common than when neither sex is exposed. Alternatively, all
male mating activity may be depressed relative to controls.
- When only the female is exposed, male mating activity will again either be
depressed or will change to less conspicuous strategies, relative to the
control situation.
- When only the male is exposed, changes in male behavior will be
significantly less marked than in either the "both exposed" or
"female exposed" situations, relative to controls.
- Predator inspection by one or both of the guppies before the courtship
trial will moderate the effect of predation risk on male mating activity.
Specifically, if inspection decreases the perception of risk, and/or if
inspectors are inherently more "bold" than other fish, then
inspection by one or both guppies will be associated with diminished effects
of predation risk on mating activity. Alternatively, if inspection increases
the perception of risk, then inspection by one or both guppies will be
associated with increased effects of predation risk on mating activity.
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METHODS |
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Guppies and predators
Guppies were descended (approximately five to eight generations) from individuals collected from a single site on the Quare River, Trinidad, as described in Reynolds and Gross (1992
). Natural predators
present at this location include the pike cichlid Crenicichla frenata
(Ploeg, 1991). We divided
approximately 100 fish (50:50 sex ratio) among 5 breeding tanks, with spawning
mops and rocks as refuges for breeding females and young. A breeding
population of at least 100 individuals was maintained throughout the study. We
removed young from these breeding tanks before their gender became
identifiable and placed them into another tank. This tank was scanned daily to
pick out sexually maturing fish. As soon as fish began showing signs of sexual
development (in fin shape, body coloration, or ovary or gonopodium growth),
they were transferred to holding tanks and reared in same-sex groups until
they were used in the experiment. This ensured that all males and females used
in the experiment were virgins. Test fish ranged from 20-25 mm total body
length (mean±SD, females: 23.38±1.53 mm; males:
21.87±1.03 mm), and each fish was tested only once. Guppies were raised on ground Tetramin flakes and live brine shrimp nauplii; adults were also fed live adult brine shrimp. Lighting was from fluorescent tubes on a 12 h:12 h light/dark cycle, and the room temperature was 30±2° C.
The two predators we used were a male and a female Crenicichla, species affinity saxatilis, both measuring 150-160 mm total body length. These were from the same species complex (saxatilis) as the natural predators, and resembled them in morphology and behavior (W. Leibel, personal communication). Predators were fed a diet of live juvenile guppies during the data collection period.
Experimental setup
The experimental setup consisted of a clear plexiglass courting tank (35 cm
x 22 cm x 16 cm deep), divided in half by a removable opaque panel
(Figure 1). This panel was
connected by monofilament to a pulley, which allowed it to be lifted out of
the tank from a remote location. Outer surfaces of the tank were white except
for the two end walls facing the predators, which were clear. The courting
tank was filled with 7 1 of water (8 cm deep) and placed at the center of the
experimental stage. We placed predator tanks (27 cmx25 cmx24 cm
deep) on either side of the courting tank, leaving gaps of <3 mm between
each. Predator tanks had opaque plexiglass on three sides, and a glass front
facing the courting tank. The outer surface of the glass front was covered by
one-way tinting film. We kept predator tank water at the same depth (8 cm) as
the courting tank. A light above each predator tank was shielded from the
courting tank by a white wooden partition. When the light above the predator
tank was on, the guppies could see the predator, but not vice versa. When the
light was off, the film on the glass prevented viewing in either direction. A
divider in each predator tank cut each tank in half during trials; depending
on the experimental treatment, the predator was positioned on one side or the
other. This allowed us to expose one, both, or neither predator to the guppies
in the courting tank, while always displaying one lit half of each predator
tank. Airstones in the predator tanks were positioned behind the divider so as
not to influence predator visibility.
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Tanks were positioned on a shelf approximately 1 m from the floor and surrounded on all sides except the top by white sheets that allowed some light through. Incident light levels within the experimental setup were 80-100 lux. A video camera was mounted 25 cm directly above the courting tank, providing a view of that tank and the front quarter of both predator tanks. The camera was connected to a VHS tape deck with which we recorded guppy activity, along with a time track. Predator exposure lights, the camera, monitor, and VHS deck were all operated from outside the experimental setup.
Experimental procedure
The day preceding a trial, we randomly selected one female and one male
guppy and placed them into opposite sides of the courting tank, with the
opaque door in place. Positioning of each fish was determined by a preset
order (see below). White card-board screens were present between the courting
tank and the two predator tanks. Lids were placed over each half to keep fish
from jumping out, and the fish were held in the courting tank until the next
morning (approximately 23 h).
We started all trials between 0830 and 0930 h. Just before the trial, lids were removed. Dividers were placed in the middle of each predator tank and predators positioned on the appropriate side of their divider wall, as determined by the experimental treatment. Next, the cardboard screens between the predator and courting tanks were removed. Four minutes later, VCR recording began.
One minute after starting the recording, we turned on both lights, exposing one, both, or neither predator to the male and female guppies. The treatment period lasted for 10 min. During this time, the video recorded the activity of the guppies and also any activity of the predator(s) near the front glass. After 10 min, the lights were switched off and the cardboard screens gently replaced between the tanks. One minute later we raised the divider in the courting tank and the courting trial began. The trial was 20 min long.
After 20 min, the video was stopped and the test guppies were captured and measured (total body length, mm) before placing them into the breeding tanks (i.e., no guppy was tested more than once). Courting tank water was removed and tank walls were scrubbed before adding fresh, conditioned water. Dividers were removed from the predator tanks, and predators were fed and their tanks cleaned if necessary. The courting tank divider was replaced and new guppies were selected and placed into the tank for the following day's trial.
We conducted four treatments in a modified Latin square design
(Table 1; Sokal and Rohlf, 1981). The
treatments consisted of control trials (in which neither sex of guppy was
exposed to a predator before the courting trial); male-exposed trials (in
which only the male saw the predator); female-exposed trials (only the female
saw the predator); and trials in which both guppies were exposed to a predator
before the courting trial. Two trials in each of these four treatments were
completed before a new cycle of trials began. In each cycle of trials, we
balanced the position of males and females to eliminate any possible bias due
to differences between the two predators or other between the two sides of the
courting tank.
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Video and data analysis
We analyzed videotapes at the end of each block of eight trials, and
behaviors were scored as described in Table
2 for each 20-min trial. After all 100 trials were completed, we
conducted statistical analyses. Data did not conform to a normal distribution,
and we therefore used nonparametric statistical analyses (Mann-Whitney
U tests). Ratios with 0 in the denominator were considered undefined
and dropped from the analysis.
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Predator inspection
The 10-min predator treatment period was also monitored and data were
recorded on the activity of the guppies while exposed to the predator(s).
Sometimes the treated guppy moved to the glass to "inspect" the
predator. This was an obvious behavior: the guppy moved to a point close to
the glass in front of the predator and oriented directly toward it. Guppies
who moved to the glass (0.5 mm or less from the glass), oriented toward the
predator, and remained there for even a short period (
1 s) during the
treatment were classified as inspectors. We then analyzed inspector and
noninspector trials separately to look for effects of inspection on responses
of mating behavior to predator exposure.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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All fish
We conducted a total of 100 trials, 25 for each test condition (controls, both fish exposed to the predator, female-only exposed, and male-only exposed). A grand total of 2,182 sigmoid displays, 638 thrusts, and 216 complete thrusts (probable matings) were observed. Courtship and mating did occur under the threat of predation, but occurred less often when only the female had seen the predator (Table 3) than in any other test condition (controls, both fish exposed, and male exposed).
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Surprisingly, predator exposure had no effect on either the ratio of thrusts to sigmoids or on our alternative index of sneaky matings, the proportion of all thrusts preceded by a sigmoid. Both measures were largely unaffected by predation risk (Figure 2). Similarly, examination of complete (potentially successful) thrusts per time spent in sigmoid displays, a plausible measure of mating success as a function of courtship investment, revealed no significant changes relative to controls for male-exposed, female-exposed or both-exposed trials (Figure 2C). Thus, sneaky matings (thrusts without sigmoid displays) were not more frequent when fish were exposed to predators.
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Other measures of mating activity were more affected by predator exposure, and these effects were most marked when only the female was exposed. For example, both the total number of sigmoid displays (Figure 3A) and the total time spent in sigmoid displays (Figure 3B) were significantly lower than controls when only the female was exposed to predation risk, but not when only the male was exposed. Time to the first thrust was significantly longer compared to controls when only females were exposed, but not when only males were exposed (control: 268.5±262.0 s, n = 25; males: 327.2±304.0 s, n = 25, ns; females: 550.0±478.3 s, n = 25, Mann-Whitney U test, p =.045). Total thrusts were also influenced by predation risk. Exposure of the female alone resulted in a significant drop in the number of thrusts (Figure 3C) compared to controls; this effect was significantly greater than when only males were exposed. The total number of thrusts was also significantly affected when both sexes were exposed to the predator. However, the number of thrusts that were complete (possibly successful) did not change significantly with predator exposure (Figure 3D).
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Comparisons of the results from male-exposed versus female-exposed trials demonstrated significant differences between the sexes in the effects of predation risk on total sigmoids (Figure 3A), total sigmoid time (Figure 3B), and total thrusts (Figure 3C). All three measures declined significantly more when only the female had been exposed to the predator than when only the male had been exposed.
Inspectors versus noninspectors
Inspection behavior, in which the guppies closely approached the glass in
front of the predator and oriented to it during some part of the exposure
period, was strongly correlated with levels of mating activity. When one or
both sexes inspected the predator, predator exposure had few effects on mating
activity. In contrast, when either the male or female (or both) was exposed to
the predator, but neither fish inspected, mating activity was depressed
relative to controls.
For example, noninspecting fish performed significantly fewer sigmoid displays than controls when either the male or female was exposed. However, inspectors showed no significant change in this measure (Figure 4). Sigmoid time declined significantly for noninspectors in male-treated trials and female-treated trials, yet in inspector trials this measure never deviated significantly from controls (Figure 4). In noninspectors the number of thrusts was significantly lower than controls for female-treated trials, but inspectors showed change in this measure only when both fish were treated (Figure 5). Also, time to the first thrust was significantly greater than controls when males or females were exposed to the predator and did not inspect (control: 268.5±262, n = 25; males: 410.9±314.0, n = 11, p =.0462; females: 688.5±486.1, n = 15, p =.0066), but not when inspection occurred.
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Again, we found no consistent evidence for a switch to a sneaky strategy. Ratios of thrusts/sigmoids for noninspectors and inspectors did not differ significantly from controls (Figure 5), and neither inspectors nor noninspectors differed significantly from controls in the proportion of thrusts preceded by a sigmoid display (not shown).
In both noninspectors and inspectors, depression of mating activity was again greatest when females alone were exposed to the predator. For example, in noninspectors, decreases in the number of thrusts (Figure 5) were significantly greater for female-treated trials (n = 15) than male-treated (n = 11) trials (p <.05). In inspector trials, the sexes also differed in the time spent in sigmoid displays (Figure 4), with female exposure yielding a larger negative effect on sigmoid time than male exposure (p =.0202; n = 10 females and 14 males).
Finally, within the noninspectors, exposure of females seemed to have longer lasting effects on some measures of mating activity than exposure of males. When only males were exposed to the predator, decreases in the number of thrusts occurred in the first 10 min of the trial, but disappeared in the second 10 min. When only females were exposed, the effect on thrusts not only began early in the trial, but persisted over the entire 20-min period (Figure 6). In contrast, decreases in sigmoids persisted over the entire trial when either sex was exposed to the predator.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Our results demonstrate that mating activity in general is depressed by exposure to a predator. Guppies showed a lower frequency of courtship and mating behaviors (sigmoid displays and thrusts) after predator exposure. Our results also show that in guppies, the effect of predator exposure is strongest when the female sees the predator. When only the male was exposed, frequencies of sigmoid displays and thrusts were diminished relative to controls. However, when only the female was exposed to the predator, sigmoid displays and thrusts were diminished even more. Additionally, effects of predator exposure on thrusts were longer lasting when females were treated, compared to the duration of effects when males were treated. Although sigmoid displays and thrusts are behaviors whose rates of performance have been attributed solely to decisions of the male guppy, our results show them to be strongly affected by the female's perception of risk. These results suggest that in this species, females may be more sensitive to predation risk than males are.
Depression of mating activity in response to predator exposure has been
found in other animals, including gobies, pipefish, salamanders, water
striders, and voles (Fuller and Berglund,
1996; Magnhagen,
1991; Ronkainen and Ylonen,
1994; Sih, 1988;
Uzendoski et al., 1993).
Moreover, other studies have hinted that female guppies may be more sensitive
than males to predation risk. Magurran and Nowak
(1991) reported that female
guppies school more than males in the presence of risk and that females also
engage in more predator inspection behavior than males, and Andreev
(1993) reported that females
are less active than males in unfamiliar environments, where higher activity
might be expected to increase vulnerability to predation.
Female behavior after predator exposure
How exactly do female guppies react to predator exposure, and how does this
affect the expression of sigmoids and thrusts by males? Although we did not
specifically study female behavior, one possibility is that females become
less active in general after predator exposure, and therefore less available
to males for courtship. For example, females in our experiments sometimes
responded to predator exposure by hugging a wall or corner of the courtship
tank and reducing their rates of movement. Presumably, such inactivity would
make a female less conspicuous to a predator, but it also could reduce her
ability to respond to males. In nature, a female might reduce her
vulnerability to predators by moving to a sheltered spot and remaining
inactive there.
Alternatively, females might actively avoid males after predator exposure,
even fleeing from the male's vicinity. This behavior has been described for
female guppies trying to avoid harassment by persistently courting males
(Magurran and Seghers, 1994),
but it has not been related specifically to predation risk. Finally, females
might be distracted by predators, especially when they are inspecting them,
and so become less receptive toward male courtship. This can then lead males
to attempt sneaky matings with them
(Magurran and Nowak, 1991).
Our data on females are not sufficiently detailed to allow us to evaluate
these various alternatives. However, in our experiments, predator inspection
before male-female interaction was not associated with a higher frequency of
sneaky matings. Also, in a laboratory study of the same guppy population that
we used (Quare River), Godin and Briggs
(1996) found that females
usually moved away from males after seeing a predator. This suggests that
active avoidance of the male by the female may have been responsible for the
changes in male behavior that occurred in our experiments. Additional data on
female behavior are needed to assess this possibility.
Male behavior after predator exposure
Contrary to expectation, males in our experiment did not switch to a
"sneaky" strategy (thrusts without displays) when they were
exposed to predation risk. Rather, the frequencies of both sigmoid displays
and thrusts declined. There are several possible reasons for this finding,
which differs from the results of previous studies (e.g.,
Endler, 1987;
Magurran and Nowak, 1991;
Magurran and Seghers, 1990).
First, in our experiments the predator was not present during courtship
trials. Guppies that were exposed to the predator before trials had to
remember it later. If males have shorter memories than females, then they
could be less affected than females by prior exposure to the predator. This
could lead to fewer sneaky matings in the male-exposed trials, although it
does not explain why both thrusts and sigmoids declined relative to controls,
nor why sigmoids remained depressed. Second, the virgin females that we used
in courtship trials are especially attractive to male guppies
(Crow and Liley, 1979). Perhaps
males perceived the risk of predation, but largely disregarded it, and
performed sigmoid displays (albeit at a lower rate than in control trials) to
ensure successful mating with virgins. Note that thrusts preceded by sigmoid
displays more often result in insemination than do sneaky matings
(uyten and Liley, 1985).
Third, the virgin males that we used in our trials may have been very highly
motivated to mate, leading them to partly disregard danger and perform sigmoid
displays (again, at a lower rate than in control trials) to ensure successful
mating. Finally, our predator stimulus was presented behind glass, and might
have been too weak to trigger sneaky mating: the predator could be seen by the
guppies, but this perception was not reinforced by other senses. Data in Godin
and Briggs (1996), collected
on the same population of guppies, also show little effect of a predator
behind glass on the thrust/sigmoid ratio, although this point is not mentioned
by the authors.
Both sexes exposed to the predator
The previous literature (e.g., Endler,
1987; Luyten and Liley,
1985; Magurran and Seghers,
1990; Reynolds et al.,
1993) had led us to believe that effects of predation risk on
mating behavior would be most apparent when both sexes experienced predation
risk, yet our data did not show this pattern. Predator inspection behavior
might account for this discrepancy between our results and those of previous
studies. Although we conducted 25 trials in which both fish were exposed to
the predator, in 21 of these trials at least one fish inspected the predator.
Because inspectors and their mating partners both showed diminished effects of
predator exposure compared to noninspectors (see below), most of the
both-exposed trials were biased (by the guppies' own behavior) against finding
significant effects.
Effects of predator inspection
Interestingly, predator inspection behavior was strongly tied to the mating
response to predator exposure. Fish that had inspected the predator (or whose
partner had inspected it) were much less likely to depress their mating
activity than fish that had not inspected. We did not have sufficient sample
sizes and statistical power to test effectively for the differential effects
of female inspection, male inspection, or inspection by both fish.
Nonetheless, the strong link we found between predator inspection and
subsequent mating behavior suggests several possible interpretations. First,
fish that inspect may be bolder individuals (sensu
Wilson et al., 1994; but see
Budaev, 1997) than those that
do not inspect. Bolder fish may be more inclined to approach the predator and
also less inclined to depress their mating activity in response to predation
risk. Moreover, if females prefer bold males, as reported by Godin and
Dugatkin (1996), then bold
males may enjoy greater mating success because of female mating
preferences.
Second, fish that inspect the predator may gain information during inspection that makes them feel safer. This could make them less inclined to change their mating activity to avoid danger. These two possible explanations for the effects of predator inspection on mating behavior merit further investigation. Because guppy pairs with only one inspector showed as little depression of mating activity as those with two inspectors, our results leave open the intriguing possibility that inspectors may in some way pass information about the predator or the level of predation risk to their mating partner.
Conclusion
Guppies have been considered a classic example showing the evolutionary
effects of predation risk on the color, morphology, and behavior of males, and
on many other life-history characters (reviewed in
Endler, 1995). Our study
demonstrates that at least some effects on male behavior with predator
exposure are indirect results of the responses of females to danger. Thus,
females mediate the effects of predation risk on male mating behavior in this
species. This suggests that females warrant more attention in this and other
mating systems where conspicuous males show variable mating strategies in the
presence of predation risk. Our work also suggests that direct effects of
predation risk on females may be important factors in constructing genetic
models for the evolution of male mating traits. Recent evolutionary models
that incorporate direct effects on females (e.g.,
Kirkpatrick, 1996;
Pomiankowski, 1987;
Pomiankowski et al., 1991)
show that these can substantially alter evolutionary outcomes. Finally, our
study shows that predator inspection by male guppies or their partners
significantly diminishes the effects of predation exposure on male courtship
and mating behavior. The mechanisms by which all of these processes occur
await further study.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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We thank John Reynolds for guppies and Ben Seghers, Richard Pocklington, and Felix Breden for discussions. This work was funded by Natural Sciences and Engineering Research Council (NSERC) Canada grant no. A6869 to L.M.D. and a President's Research Award from Simon Fraser University to L.M.D. and A.V.H. A.V.H. was supported by an NSERC Canada International Postdoctoral Fellowship during part of this study.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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