Behavioral Ecology Vol. 11 No. 4: 444-451
© 2000 International Society for Behavioral Ecology
Courtship displays and coloration as indicators of safety rather than of male quality : the safety assurance hyposthesis
a Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA 93106, USA b Behavioural Ecology Research Group, Department of Biological Sciences, Simon Fraser University, Burnaby, BC V5A 1S6, Canada
Address correspondence to R. R. Warner. E-mail : warner{at}lifesci.ucsb.edu .
Received 20 December 1999; accepted 27 December 1999.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Male courtship displays and bright coloration are usually assumed to provide information to females about some aspect of the male's value as a mate. However, in some species, courtship may serve another function—namely, indicating the current predation risk at the mating site and assuring the female that it is safe to mate there at this time. We developed this safety assurance hypothesis (SAH) and tested its predictions in the bluehead wrasse (Thalassoma bifasciatum), a Caribbean reef fish. Females in this species come to males' territories to spawn, and males court each arriving female. Males with larger white flank patches court less intensely than less bright males. We show that such males are probably more visible to predators and thus need not court so intensely to provide the same degree of safety assurance to a female. When model lizardfish predators are presented at spawning sites, males habituate to them quickly, but newly arriving females who see the predator are expected to demand more assurance of site safety. Accordingly, and consistent with the SAH, males court females more intensely (longer average courtship bout length) under such circumstances, but males with bright flank patches do not increase their courtship as much as duller males do. Despite this relatively low intensity of courtship, the spawning rate of bright males does not decline relative to that of duller males in the presence of a predator, suggesting that bright coloration conveys a differential benefit. Females of species like the bluehead wrasse, who spawn repeatedly over the course of their life, are expected to be more concerned with their own risk of mortality during each spawning bout than with the quality of a particular male. It is in such species that we expect the SAH to be most applicable.
Key words: bluehead wrasse, coral reefs, courtship behavior, fish, risk aversion, safety.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Courtship displays and coloration have traditionally been viewed as means for the male to convey information about himself to the female (Alcock, 1998
;
Andersson, 1994 ;
Hamilton and Zuk, 1982). This
may include information on species identity and individual quality. In species
where the male subsequently provides care for the young, courtship intensity
has been shown to correlate strongly with quality of care (e.g.,
Greig-Smith, 1982 ;
Knapp and Kovach, 1991 ;
Sikkel, 1995), and brightly
colored males in some species have been shown to be in better condition than
less brightly colored ones (Milinski and
Bakker, 1990). Even in species without male parental care, there
is some evidence that courtship may convey information about indirect benefits
accruing to mates (e.g., Reynolds and
Gross, 1992).
However, courtship occurs in some situations where it would appear that
females would not require further information about a prospective mate.
Consider the bluehead wrasse (Thalassoma bifasciatum), a common fish
inhabiting shallow water over coral reefs throughout the Caribbean. Mating
takes place year round, and individual females mate several times per week.
These females tend to be highly faithful to particular mating sites (Warner,
1987,
1990), where the same brightly
colored male will be present for an average of about 90 days and sometimes
much longer (Hoffman et al.,
1985). Individual males are easily distinguished by variability in
a distinctive black-white-black marking on their flanks, and it has been shown
that females respond to this coloration character
(Warner and Schultz, 1992).
Yet, each time the female arrives on the site to mate, the male courts her
assiduously. There is no parental care in this species. Why must the male
court the female ? A proximate ethological explanation is that courtship and
coloration are necessary to stimulate and otherwise prepare a female for
mating (e.g., Crews, 1975,
1992). Such is not the case for
the bluehead wrase : at other mating sites large males are displaced by
group-mating aggregations of smaller, less brightly colored males, and females
mate readily at these sites without benefit of courtship
(Warner and Hoffman,
1980a).
Here we propose and test a hypothesis about an alternative function of
courtship and bright male coloration : the safety assurance hypothesis
(Warner, 1987 ; see also
Uzendoski et al., 1993). We
suggest that under certain circumstances the information conveyed concerns
safety of the mating site rather than some characteristic of the male himself.
That is, females may still require information before mating, but their mating
decisions may be based more on current site safety (a transient quality) than
on the relative quality of the male. We tested the safety assurance hypothesis
(SAH) by manipulating female perceptions of local safety and observing male
courtship responses.
The SAH suggests that bright coloration and intense courtship convey more information to a female precisely because they are dangerous. If a brightly colored male is more detectable by a predator than a dull male, then all else being equal, the presence of the bright male conveys relatively greater assurance of current local safety to the female. A similar argument can be made for courtship : if longer or more intense courtship is more dangerous, then a male conducting such a bout will convey more information about current safety to an observing female than would a male conducting a shorter, less intense courtship bout. If both coloration and courtship serve to convey safety information, a brightly colored male will be able to court less than a dull male and still convey safety assurance information, while a dull male will be required to court more. We tested this corollary of the SAH by examining male courtship in relation to their coloration and by measuring the response of differently colored males to changes in female perception of local safety.
To illustrate this idea and to introduce the research setting, we continue
with our example of the bluehead wrasse. Courtship by brightly colored males
is conspicuous and occurs in the area (high in the water column) where mating
will occur. Release of gametes from high in the water column can aid in
conveying fertilized eggs away from reef-based predators and may aid dispersal
as well (Randall and Randall,
1963 ; Robertson and Hoffman,
1977 ; Thresher,
1984). However, the risk of predation on adults increases with
distance from the protection of the reef
(Hobson, 1975), and the mating
act itself reduces vigilance. Mating in many animals increases predation risk
(Endler, 1983 ;
Gwynne, 1989 ;
Lima and Dill, 1990 ;
Magnhagen, 1991 ;
Ryan, 1985), and courtship is
often performed near where mating will occur. Bright coloration may also
increase predation risk (Endler,
1991), both for the bright male and the attending female
(Pocklington and Dill, 1995).
Thus females may mate with certain males because doing so reduces the
predation risk cost of mating
(Clutton-Brock et al., 1993 ;
Deutsch and Weeks, 1992). Here
we extend this idea by suggesting that courtship and coloration can provide
females with information about current predation risk, even after mate choice
has occurred.
In the bluehead wrasse, the qualities of the courting male are not likely
to change over the course of several days : size, coloration, behavior, and
sperm output are relatively invariant
(Hoffman et al., 1985 ;
Warner and Hoffman, 1980b ;
Warner et al., 1995a).
However, the current safety of the mating site can change dramatically.
Predators such as lizardfish, groupers, and snappers tend to range widely, and
an element of surprise is often essential to their success
(Hobson, 1975). The fact that
a predator was not present at some previous time may have no information value
as to the present safety of a mating site. For a female, a simple
demonstration of the current safety of a mating site could be much more
important to fitness than information about a particular male, and male
displays could provide such a demonstration. The SAH predicts that the
addition of obvious potential predators should alter the apparent quality of
the site and induce females to require more assurance of safety, perhaps
through more courtship or other conspicuous behavior. However, if courtship or
coloration is simply a means to convey information about the male, there
should be no change in behavior, or activity should decline because of the
risk to males. In the following experiments, we attempted to disentangle male
and female interests by temporally separating the apparent predation threat to
the two sexes.
To be applied to the bluehead wrasse, the SAH encompasses a series of assumptions and predictions, each of which were tested : (1) Males designated as conspicuous are indeed easier for predators to detect visually. (2) Courtship behavior is dangerous. Males under predation threat will curtail courtship. (3) Females require safety assurance before mating. Given an existing amount of information about the male, females under greater predation threat will require more courtship. (4) If both conspicuousness and courtship are effective at conveying safety information to a female, then under normal conditions females will require less courtship from bright males. Thus, courtship intensity and coloration will be inversely related. Under predation threat (perceived by females, but not males), less conspicuous males will increase courtship activity more than bright males.
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
This study took place on patch reefs in Tague Bay, St. Croix, U.S. Virgin Islands (17°45' N, 64°35' W), May-July 1995 and 1996. Thalassoma bifasciatum is dichromatic : large males are in the terminal color phase (TP), easily distinguished from the less conspicuous initial color phase (IP) of females and smaller males. On Tague Bay patch reefs, most females feed on plankton on the upcurrent ends of reefs during the day and migrate to specific downcurrent mating sites for a single, brief visit (Warner and Schultz, 1992
).
Individual TP males each occupy a spawning site
(Hensley et al., 1994 ;
Warner, 1988) and defend the
site against smaller, younger IP males
(Warner, 1984 ;
Warner and Hoffman, 1980b).
Mating takes place daily during a discrete afternoon period of about 3 h,
throughout the year. For the following experiments, a critical aspect of the
mating system is that females arrive sequentially at the mating site so that
the brief individual visits are spread over the mating period, with few or no
interactions occurring among females. Fertilization is external and the eggs
are pelagic, so neither males nor females have any further contact with the
young. Previous studies of tagged individual females indicate that, on
average, they spawn 2 out of every 3 days and strongly tend to return to the
same mating site (Warner,
1984,
1986,
1995). This fidelity leads to
consistent differences between TP male sites in average daily spawning rates,
from less than 5 to more than 80 matings per day
(Warner et al., 1995a).
As mentioned above, TP males have a distinctive black-white-black flank
patch on their sides (see vignette in
Figure 1). The proportion of
white in this flank patch has been shown to be positively correlated with both
female preference for particular males and with successful TP male defense
against smaller males ; the overall size of the patch had a much weaker effect
(Warner and Schultz, 1992).
This flank patch is variable between individuals but cannot be modified in
size by an individual except through scale replacement, which can take several
weeks. Predictions of the SAH would be more complex if bright coloration were
correlated with a male's intrinsic ability to escape predation. In the
bluehead wrasse, however, the proportion of white in the flank patch is not
correlated with morphometric variables in territorial TP males, including
depth of body, overall length, or relative pectoral fin length
(Warner and Schultz,
1992).
|
To gauge the contribution of the flank patch to conspicuousness of the
male, we constructed nine two-dimensional models of TP males. These models
were the size of an average-length TP male [90 mm standard length (SL)] and
differed in the overall size and percent white of the flank patch. The total
width of the patch varied from narrow (10 mm), to medium (15 mm), to wide (20
mm). In nature, the average width of flank patches at the lateral line is 16.2
mm. Within each width category, the percent white was either 15%, 25%, or 50%
; average percent white in nature is 23.3%
(Warner and Schultz, 1992).
Conspicuousness was judged by a human observer as the maximum distance (in
meters) at which the flank patch could be seen under water. All models were
tested 5 times on each of 5 different days. Visibility naturally varied
between days, and we normalized each day's results relative to the daily mean
sighting distance for the set of nine models. We do not assume that marine
predators have the same visual abilities as a human being with a facemask, but
rather seek to estimate the relative conspicuousness of different intensities
of the flank patch markings.
We attempted to distinguish between alternative functions for courtship and coloration by observing the relationship between these two variables in a natural setting. We also manipulated perceived predation risk through controlled presentation of a model predator. At the beginning of the presentation, both the male and any females present presumably perceive the model as a threat. As the spawning period progresses, the male gains information that this particular predator is not a threat (i.e., the male habituates). In contrast, females are present sequentially at the spawning site for only short periods of time, and thus each female perceives the threat anew.
For each of 17 experiments, two mating sites on the same large reef were
chosen as a pair. Members of the pair were closely matched as to average daily
mating success, rate of intrusion by smaller males, and physical
characteristics of the spawning site (see
Warner, 1988). During the
experiment, each site of the pair was observed for the same 2 days for the
entire spawning period (approximately 3 h). The observer at each site
continuously recorded all spawning and courtship behaviors. Bluehead wrasse
courtship was consistent and stereotypical. The male positioned himself in the
water column 0.5-1.5 m above the spawning site and the waiting female. He
would then swim in very tight circles, rapidly vibrating his pectoral and
caudal fins (Dawkins and Guilford,
1994). During courtship, the tips of the vibrating pectorals were
black (normally they were clear). We defined a courtship bout by continuous
fin vibration ; if a male paused for more than 1 s, we considered the bout
terminated. The initiation time and duration of every courtship bout was
recorded. In most cases, courtship was eventually followed by spawning : the
female would begin to rise in the water column and would be joined by the male
as she rapidly accelerated toward the surface. At the apex of the rapid
spawning rise, the female released all of her eggs simultaneously with sperm
release by the male, and both fish then moved quickly back to the substrate.
The entire spawning sequence took less than 1 s, and fertilization was
completed in the water column in less than 15 s
(Petersen et al., 1992 ;
Warner et al., 1995a).
Courtship was occasionally accompanied by repeated upward dashes of the male
("loops") that mimic the spawning rush.
Courtship intensity can be expressed as a rate (number of courtship bouts per spawn) or as a duration (average courtship bout length). Although courtship duration changed dramatically in the presence of the model (see below), there was no discernable effect of the predator addition on overall courtship rate (mean ± 1 SE courts per spawn in control series, 2.80 ± 0.22 ; experimental series, 2.74 ± 0.25 ; paired t test, n = 34 pairs, t = 0.19, p =.85). Thus only courtship duration is discussed below.
On the first day of an experimental series, one of a pair of mating sites was randomly designated as the experimental site. At the base of this mating site we placed a Plexiglas cylinder (12.8 cm diam, 61 cm long) containing a preserved lizardfish (a sand diver Synodus intermedius, 39 cm standard length) on a 2 cm bed of sand. Lizardfish (Synodidae) are sedentary, benthic predators that attack from positions on the bottom. They account for the majority of the attacks on blueheads during spawning (174 of 256 predation events witnessed in Panama and St. Croix since 1974 ; Warner RR, personal observation). The lizardfish was coated with clear epoxy resin and positioned in a realistic posture. When presented with the model predator inside the cylinder, blueheads at the experimental sites showed cautious behavior (see Results). The cylinder prevented close inspection of the model and resulted in a measurable habituation period (see below). At control sites (the other member of the pair), we deployed an identical but empty Plexiglas cylinder. On the second day of the experimental series, the deployments were reversed. Thus in half of the comparisons, the control presentation preceded the experimental one, while in the other half the experimental presentation was done first. Subsequent analysis revealed no effect of the order of presentation.
After half of the 2-day experimental series, TP males were captured,
measured, and photographed. We recorded standard length, body depth, tail
length, and pectoral length from the fish themselves (see
Warner and Schultz, 1992).
From digitized images, we recorded the relative area of white in the flank
patches. For any paired structure, the two measurements were averaged. Because
of logistical difficulties, measurement and recapture were not initiated until
late in the 1995 series. Of the 34 males used in the experiments, 17 were
captured for these measurements (4 of 20 in 1995 and 13 of 14 in 1996).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Conspicuousness as a function of coloration
Our observations of fish models revealed that, in general, conspicuousness of the flank patch increased with the overall width of the patch and with the percent of white within the patch (Figure 1, Table 1). While visibility increased consistently with the total width of the patch, the percent white in the patch strongly affected visibility only when increased from 15% to 25% (Figure 1). There was little or no additional contribution to visibility due to increases of percent white from 25% to 50% (individuals in the experimental series naturally ranged between 16% and 28% white ; see Figure 2). The interaction between patch width and percent white was not significant (Table 1), indicating that an increase in percent white had a similar effect regardless of the actual size of the flank patch. The overall average maximum distance at which flank patches could be seen by a human was 9.4 m, which is substantially larger than the radius of a typical TP male mating terrotory (Warner and Hoffman, 1980b
).
|
|
Relationship of courtship duration to male coloration
Under control conditions, males varied in average courtship duration, and
there was a clear relationship of this duration with the percent of white in
the flank patch (Figure 2).
Males with a greater percentage of white in their patch tended to court for
shorter durations (r = -.742, p <.001).
This result is consistent with the idea that courtship and coloration may
both serve to convey information to a female and that one may substitute for
another. However, the basis for variation among males could be due to another
causal variable. The most obvious candidate is daily mating rate because this
varies greatly between males (Hoffman et
al., 1985 ; Warner and
Schultz, 1992). Daily mating rate is known to affect sperm output
per spawn (Warner et al.,
1995a), so it was quite possible that it could affect courtship
intensity as well. Increases in mating success are also known to be associated
with large amounts of white in the flank patch of the TP male
(Warner and Schultz, 1992).
However, there was no relationship between the total number of spawns accrued
by a male on the control day and his mean courtship duration (r =.13,
p >.50). In a related study using many more males, Warner and
Schultz (1992) also found no
correlation between average daily mating success and mean courtship duration.
There was also no relationship between mean courtship duration and any of the
morphometric variables (n = 17, p >.05 for standard length, body
depth, tail length, and pectoral length).
General effects predator addition
The presence of the model predator at the mating site resulted in a strong
initial reaction by both male and female bluehead wrasses. The same behavior
was shown by males before habituation (see below) and by females subsequently
arriving at the mating site. Individuals would remain quite near the
substrate, oriented head-on toward the model. Fish would often slowly approach
the model, swimming in a characteristic up-and-down motion as they came closer
to the model (see Godin and Davis,
1995, for an example of how such behavior reduces predation risk).
Blueheads react in an identical fashion under normal situations when a
predation threat is present (Warner RR, unpublished observations). The
presence of the cylinder without the model elicited no such reaction. Bluehead
wrasses are opportunistic feeders, and the addition of the empty cylinder
resulted in immediate inspection. Subsequently it was ignored.
While there was no question that the model was treated with caution, there
was only a slight overall effect of predator addition on overall spawning rate
at a particular site (Figure
3). The mean spawning total on predator-addition days was 91% of
that on control days, indicating that most females did not simply abandon
mating at a site with predation threat. As suggested by the results presented
above, there was no relationship between losses of mating and male coloration,
morphometric, or behaviro variables. While between-site variation is
considerable, spawning rates at a particular site normally remain rather
constant from day to day, with an average coefficient of variation of 26%
(Warner and Schultz, 1992).
The fact that females detected the predator but continued to spawn at the site
allows an investigation of male response to females, as presented below.
|
Effects of predator addition on courtship
Initial responses of males
There was a strong initial response of courtship duration to predator
addition. For all males, courtship duration was initially short, averaging
less than 45% of the duration of courtship in the initial periods of the
control observations for the same males (mean ± 1 SE courtship duration
in first 10 min of spawning : control, 4.2 ± 0.2 s ; with predator, 1.9
± 0.3 s ; p <.001). Courtship responses are most easily
visualized as average courtship durations for successive 5-min periods over
the course of the spawning period (examples in
Figure. 4). Courtship duration
remained depressed for an average of 2.4 5-min periods before it returned to
control levels (or greater, see below), showing a clear pattern of
habituation. Thus we did not use the first two time periods in the calculation
of post-habituation responses, either in the controls or the experimental
presentations (below).
|
Subsequent responses of males
After the habituation period, males varied considerably in their courtship
responses. For many males (e.g., Figure 4a
and 4b), the courtship durations increased after habituation to
levels much higher than in the control situation and remained high during the
entire spawning period. For other males, however, courtship durations only
returned to control levels (e.g., Figure
4c).
Overall, the posthabituation courtship response had a distinct pattern relative to control levels of courtship duration (Figure 5). Males with relatively short average courtship durations on control days showed little or no posthabituation response to predator addition, whereas males with long mean courtship durations in the control tended to be those who increased courtship duration in the presence of a predator. The regression relationship between control mean courtship durations (CC) and mean courtship durations with a predator present (PC) was PC = (2.73) CC - 5.11. The 95% confidence interval for the slope was between 2.25 and 3.20, indicating a strong tendency for larger responses by males with longer control courtship durations. The regression crosses the 1:1 line at a mean courtship duration of approximately 3 s ; thus males with average control courtship durations less than this value showed little or no post-habituation response to the model's addition.
|
Response to predator addition as a function of coloration
Once habituated, males tend to increase courtship durations in the presence
of a predator, if they respond at all. The males that do respond are those
that have relatively long courtship durations in the absence of a predation
threat. These are the males with relatively small amounts of white in their
flank patches (Figure 2). Given
this relationship between coloration and courtship duration, the pattern of
posthabituation response to the addition of the predator model becomes more
clear. Males with larger percentages of white in their flank patches not only
tend to court for shorter durations, but they also tend not to respond to the
addition of the predator model (Figure
6). In contrast, males with less white in their flank patch court
for relatively long durations and respond to predator additions by lengthening
courtship durations still further in the posthabituation period. Despite the
fact that brightly colored males had relatively lower courtship than dull
males in the presence of predators, they did not suffer any greater losses of
mating.
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
The results and their interpretation can be summarized as follows :
- Models of males with relatively large white flank patches are more
conspicuous, at least to human observers.
- All males initially court less in the presence of a predator, and thus
courtship intensity is a reliable signal indicating site safety.
- After a short period of habituation, some males increase average courtship
durations in the presence of a predator, while other males simply return to
control levels ; this suggests that females may require more intense courtship
in dangerous situations.
- Males that increase courtship duration are those with relatively long
average courtship durations during control periods.
- Males with relatively large white flank patches have relatively short
control courtship durations and respond less strongly to the predator
additions. Thus females may require more courtship from less conspicuous
males.
In other words, conspicuous males courted for shorter periods under normal
conditions and did not tend to change their posthabituation courtship duration
when females at the mating site were presented with an apparent predation
threat. In contrast, less conspicuous males courted for longer durations under
control conditions and increased those courtship durations dramatically (after
habituation) when a predation threat was added. These results are consistent
with our predictions based on the SAH, and lend themselves to the following
interpretation : Females require information about the current safety of the
mating site before mating. If this information comes from courtship activity,
males must court more if a site appears dangerous to the female. Courtship
activity is particularly reliable information when it comes from a conspicuous
male because he is more at risk to predation. These males need to court less
for the same effect. For the same reason, in the presence of predators, less
conspicuous males must increase their courtship duration more than conspicuous
males (cf. Reynolds,
1993).
Note that our interpretation of courtship and coloration implies a basic
sexual conflict rather than a strictly beneficial exchange of information
(Rowe et al., 1994). The SAH
suggests that long courtship bouts and bright coloration are inherently
dangerous, raising the risk of predation on the participating male. Because of
this risk, they convey valuable and truthful information to the female, and
this in turn increases her probability of mating. The male is willing to incur
risk because of this increased probability of mating, but his optimal strategy
would be to mate without courting or displaying bright coloration. In the
sense that bright coloration and extended courtship are risky to the male,
they are handicaps (sensu Zahavi,
1992). However, handicaps supposedly convey information to the
female about the quality of the male, while the SAH suggests that the
information concerns local safety. It is important to note that courtship is
not required at group spawn sites. In these circumstances, there are often
hundreds of other individuals present at the mating site, and the per capita
risk of predation is substantially reduced due to dilution
(Krause and Godin, 1995). In
other words, where the risk is lessened, courtship is not required.
We stress that the predictions based on safety indicators are exactly
opposite to those based on more traditional interpretations of courtship and
color. In this latter view, females should be less discriminating (and thus
require less courtship or display coloration) in the presence of a predator
(reviewed in Sih, 1994 ; see
also Hedrick and Dill, 1993 ;
Godin and Briggs, 1996).
An alternative explanation for the intensification of courtship in the presence of a predation threat would be that females are simply more reticent to spawn and become more willing to mate after a period of no attack. This would be a plausible explanation if the response were uniform across all sites (i.e., if courtship were extended at all sites in the presence of the model), or varied randomly across sites (perhaps reflecting variation between sites in the effectiveness of presentation of the model). Instead, the courtship response varied nonrandomly between sites, depending on the conspicuousness of the attending male. Thus male-female interactions under a predation threat are not independent of the male's appearance and activity at the mating site. Simple female reticence cannot explain the apparent trade-off between coloration and courtship in attending males.
Working with guppies (Poecilia reticulata), Reynolds
(1993) also noted a difference
in the courtship response of attractive and unattractive males to a perceived
predation threat. Large male guppies, which are preferred by females,
decreased their courtship more than did small ones when light levels were
increased. Although the overall response was the opposite to that seen in the
bluehead wrasse (where courtship increased under predation threat), Reynolds's
hypotheses about the reasons behind the guppies' differential response offer
an interesting alternative to the SAH. For bluehead wrasse males, Reynolds's
differential-cost hypothesis would suggest that conspicuous males cannot
afford to increase courtship because it is more dangerous for them to do so.
The prediction from this hypothesis is that attractive males would then lose
relatively more matings under predation threat than would small males. In
contrast, the bluehead version of Reynolds's differential-benefit hypothesis
suggests that conspicuous males do not increase courtship under predation
threat because they are already sufficiently attractive and extra courtship
will not increase their mating rate. Under this hypothesis, no differential
loss in mating rates is predicted.
For guppies, Reynolds found that large males lost proportionally more matings than did small males under predation threat, supporting the differential-cost hypothesis. For the bluehead wrasse, while there was a small overall decrease in mating rates when predators were present, this decrease was unrelated to male coloration or change in courtship duration. Thus this work lends support to a hypothesis based in differential benefit. In fact, Reynolds's differential-benefit hypothesis is congruent with the interaction between coloration and courtship in the bluehead wrasse, with the interesting difference that the benefits are also conveyed to the female in the form of safety assurance.
Obviously, we do not expect the SAH to apply to every situation where males
are brightly colored or display intense courtship. It is useful to consider
the circumstances under which survival considerations might take precedence
over other benefits of careful mate assessment. Life-history theory suggests a
reason that female bluehead wrasses appear more concerned with safety than
with the qualities of the particular male with whom they are to mate
(Warner, 1998). In this
sex-changing species, individuals may expect to reproduce approximately 500
times as a female in the first 2 years of their lives, and, if they survive to
become successful terminal phase individuals, to achieve another 2300 matings
as a male (Warner, 1984). For
highly iteroparous species (that is, species with many reproductive events
over the course of their lives), each particular reproductive event
constitutes a rather small proportion of an individual's total lifetime
reproductive success. In such species, survival to future reproductive events
is an extremely important component of fitness—much more important than
a marginal increase in current reproductive success
(Mertz, 1971 ;
Schaffer, 1974 ; Stearns,
1976,
1992).
In other words, individuals in highly iteroparous species will be expected
to avoid mortality risks and seek assurance that any current reproductive
activity is safe. By the same token, such individuals will not be expected to
engage in mate assessment or mate searching to the same degree as less
iteroparous species, especially if these activities involve increased risk of
mortality (Warner, 1998).
Although a great deal of attention has been paid to the potential benefits of
mate choice (e.g., Janetos,
1980 ; Reynolds and Gross,
1990), we have only recently begun to appreciate the effects of
costs (Hedrick and Dill, 1993
; Pocklington and Dill, 1995 ;
Real, 1990,
1991 ;
Sih, 1994 ;
Warner et al., 1995b). These
costs will be overwhelmingly important to species such as the bluehead
wrasse.
|
ACKNOWLEDGEMENTS |
|---|
This work was supported by the U.S. National Science Foundation (IBN95-07178 to R.R.W.) and Natural Sciences and Engineering Council Canada (grant A6869 to L.M.D.). Thanks to S. and E. Dill, D. Fitch, J. Wilson, M. Sheehy, and L. Wooninck for field assistance, and to J. Reynolds and D. F. Westneat for insightful comments.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Alcock J, 1998. Animal behavior : an evolutionary approach, 6th ed. Sunderland, Massachusetts : Sinauer Associates.
Andersson M, 1994. Sexual selection. Princeton, New Jersey : Princeton University Press.
Clutton-Brock T, Deutsch JC, Nefdt. RJC, 1993. The evolution of ungulate leks. Anim Behav 46: 1121-1138.
Crews D, 1975. Psychobiology of reptilian
reproduction. Science 189:
1059-1065.
Crews D, 1992. Behavioural endocrinology and reproduction : an evolutionary perspective. Oxford Rev Reprod Biol 14: 303-370.
Dawkins MS, Guilford T, 1994. Design of an intention signal in the bluehead wrasse (Thalassoma bifasciatum). Proc R Soc Lond B 257: 123-128.
Deutsch JC, Weeks P, 1992. Uganda kob prefer
high-visibility leks and territories. Behav Ecol
3: 223-233.
Endler JA, 1983. Natural and sexual selection on color patterns in poeciliid fishes. Environ Biol Fish 9: 173-190.
Endler JA, 1991. Variation in the appearance of guppy color patterns to guppies and their predators under different visual conditions Vision Res 31: 587-608.[ISI][Medline]
Godin J-GJ, Briggs SE, 1996. Female mate choice under predation risk in the guppy. Anim Behav 51: 117-130.
Godin J-GJ, Davis SA, 1995. Who dares, benefits : predator approach behaviour in the guppy (Poecilia reticulata) deters predator pursuit. Proc R Soc Lond B 259: 193-200.
Grieg-Smith PW, 1982. Song-rates and parental care by individual male stonechats (Saxicola torquata). Anim Behav 30: 245-252.
Gwynne DT, 1989. Does copulation increase the risk of predation ? Trends Ecol Evol 4: 54-56.
Hamilton DW, Zuk M, 1982. Heritable true fitness and
bright birds : a role for parasites ? Science
218: 384-386.
Hedrick AV, Dill LM, 1993. Mate choice by female crickets is influenced by predation risk. Anim Behav 46: 193-196.
Hensley DA, Appeldoorn RS, Shapiro DY, Ray M, Yurigan RG, 1994. Egg dispersal in a Caribbean coral reef fish, Thalassoma bifasciatum. I. Dispersal over the reef platform. Bull Mar Sci 54: 256-270.
Hobson ES, 1975. Feeding patterns among tropical reef fishes. Am Sci 63: 383-392.
Hoffman SG, Schildhauer MP, Warner RR, 1985. The costs of changing sex and the ontogeny of males under contest competition for mates. Evolution 39: 915-927.
Janetos AC, 1980. Strategies of female mate choice : a theoretical analysis. Behav Ecol Sociobiol 7: 107-112.
Knapp RA, Kovach J, 1991. Courtship as an honest
indicator of male parental quality in the bicolor damselfish, Stegastes
partitus. Behav Ecol 2:
295-300.
Krause J, Godin J-GJ, 1995. Predator preferences for attacking particular prey group sizes : consequences for predator hunting success and prey predation risk. Anim Behav 50: 465-473.
Lima SL, Dill LM, 1990. Behavioral decisions made under the risk of predation : a review and prospectus. Can J Zool 68: 619-640.
Magnhagen C, 1991. Predation risk as a cost of reproduction. Trends Ecol Evol 6: 183-186.
Mertz DB, 1971. The mathematical demorgraphy of the California condor population. Am Nat 105: 437-453.
Milinski M., Bakker TCM, 1990. Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344: 330-333.
Petersen CW, Warner RR, Cohen S, Hess HC, Sewell AT, 1992. Variation in pelagic fertilization success : implications for production estimates, mate choice, and the spatial and temporal distribution of spawning. Ecology 73: 391-401.
Pocklington R, Dill LM, 1995. Predation on females or males : who pays for bright male traits ? Anim Behav 49: 1122-1124.
Randall JE, Randall HA, 1963. The spawning and early development of the Atlantic parrotfish, Sparisoma rubripinne, with notes on other scarid and labrid fishes. Zoologica 48: 49-60.
Real L, 1990. Search theory and mate choice. I. Models of single-sex discrimination. Am Nat 136: 376-404.
Real L, 1991. Search theory and mate choice. II. Mutual interaction, assortative mating, and equilibrium variation in male and female fitness. Am Nat 138: 901-917.
Reynolds JD, 1993. Should attractive individuals court more ? Theory and a test. Am Nat 141: 914-927.
Reynolds JD, Gross MR, 1990. Costs and benefits of female mate choice : Is there a lek paradox ? Am Nat 136: 230-243.
Reynolds JD, Gross MR, 1992. Female mate preference enhances off-spring growth and reproduction in a fish Poecilia reticulata. Proc R Soc Lond B 250: 57-62.
Robertson DR, Hoffman SG, 1977. The roles of female mate choice and predation in the mating systems of some tropical labroid fishes. Z Tierpsychol 45: 298-320.
Rowe L, Arnqvist G, Sih A, Krupa JJ, 1994. Sexual conflict and the evolutionary ecology of mating patterns : water striders as a model system. Trends Ecol Evol 9: 289-293.
Ryan MJ, 1985. The túngara frog : a study in sexual selection and communication.. Chicago : University of Chicago Press.
Schaffer WM, 1974. Selection for optimal life histories : the effects of age structure. Ecology 5: 291-303.
Sih A, 1994. Predation risk and the evolutionary ecology of reproductive behavior. J Fish Biol 45 (suppl A) : 111-130.
Sikkel PC, 1995. Effects of nest quality on male courtship and female spawning-site choice in an algal-nesting damselfish. Bull Mar Sci 57: 682-689.
Stearns SC, 1976. Life history tactics : a review of the ideas. Q Rev Biol 51: 3-47.[Medline]
Stearns SC, 1992. The evolution of life histories. Oxford : Oxford University Press.
Thresher RE, 1984. Reproduction in reef fishes. Neptune City, New Jersey : TFH Publications.
Uzendoski K, Maskymovitch E, Verrell P, 1993. Do the risks of predation and intermale competition affect courtship behavior in the salamander Desmognathus ocrophaeus ? Behav Ecol Sociobiol 32: 421-427.
Warner RR, 1984. Deferred reproduction as a response to sexual selection in a coral reef fish : a test of the life historical consequences. Evolution 38: 148-162.
Warner RR, 1986. The environmental correlates of female infidelity in a coral reef fish. In : Indo-Pacific fish biology : Proceedings of the Second International Conference on Indo-Pacific Fishes. (Uyeno T, Arai R, Taniuchi T, Matsuura K, eds). Tokyo : Ichthyology Society of Japan; 803-810.
Warner RR, 1987. Female choice of sites versus mates in a coral reef fish, Thalassoma bifasciatum. Anim Behav 35: 1470-1478.
Warner RR, 1988. Traditionality of mating-site preferences in a coral-reef fish. Nature 335: 719-721.
Warner RR, 1990. Male versus female influences on mating site-determination in a coral reef fish. Anim Behav 39: 540-548.
Warner RR, 1995. Large mating aggregations and daily long-distance spawning migrations in the bluehead wrasse, Thalasoma bifasciatum. Environ Biol Fish 44: 337-345.
Warner RR, 1998. The role of extreme iteroparity and risk-avoidance in the evolution of mating systems. J Fish Biol 53 (suppl A) : 82-93.
Warner RR, Hoffman SG, 1980a. Local population size as a determinant of mating system and sexual composition in two tropical marine fishes (Thalassoma spp.) Evolution 34: 508-518.
Warner RR, Hoffman SG, 1980b. Population density and the economics of territorial defense in a coral reef fish. Ecology 61: 772-780.
Warner RR, Marconato A, Shapiro DY, Petersen CW, 1995a. Sexual conflict : males with highest mating success convey the lowest fertilization benefits to females. Proc R Soc Lond B 262: 135-139.[Medline]
Warner RR, Schultz ET, 1992. Sexual selection and male characteristics in the bluehead wrasse, Thalassoma bifasciatum : mating site acquisition, mating site defense, and female choice. Evolution 46: 1421-1442.
Warner RR, Wernerus F, Lejeune P, van den Berghe EP,
1995b. Dynamics of female choice for parental care in a species
where care is facultative. Behav Ecol 6:
73-81.
Zahavi A, 1992. Sexual selection—badges and signals. Trends Ecol Evol 7: 30-31.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  I. M. Hamilton, M. P. Haesler, and M. Taborsky Predators, reproductive parasites, and the persistence of poor males on leks Behav. Ecol., January 1, 2006; 17(1): 97 - 107. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. J. Murphy Context-dependent reproductive site choice in a Neotropical frog Behav. Ecol., September 1, 2003; 14(5): 626 - 633. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Semsar and J. Godwin Social Influences on the Arginine Vasotocin System Are Independent of Gonads in a Sex-Changing Fish J. Neurosci., May 15, 2003; 23(10): 4386 - 4393. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Montgomerie, B. Lyon, and K. Holder Dirty ptarmigan: behavioral modification of conspicuous male plumage Behav. Ecol., July 1, 2001; 12(4): 429 - 438. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Taborsky The Evolution of Bourgeois, Parasitic, and Cooperative Reproductive Behaviors in Fishes J. Hered., March 1, 2001; 92(2): 100 - 110. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||