Behavioral Ecology Vol. 10 No. 4: 366-371
© 1999 International Society for Behavioral Ecology
Are males with more attractive resources more selective in their mate preferences? A test in a polygynous species
a Department of Biological Sciences, 31 Williams Hall, Lehigh University, Bethlehem, PA 18015, USA b Discovery Bay Marine Laboratory, University of the West Indies, Discovery Bay, Jamaica
Address correspondence to M. Itzkowitz. E-mail: MI00{at}lehigh.edu
Received 8 April 1998; revised 30 July 1998; accepted 25 November 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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In many polygynous species, males typically direct more intense courtship toward more fecund females. Here we examined this behavior in relation to the attractiveness of a male's resource. We used the territorial polygynous beaugregory damselfish (Stegastes leucostictus) and manipulated the quality of male breeding territories with two types of artificial sites. We also investigated variable natural breeding territories. Previous studies have shown that these different breeding sites were of different qualities, as judged by the number of eggs accrued by the defending male. Males on all three types of breeding sites did court females, and males using the highest quality sites exhibited significantly higher courtship intensity. However, only the group of males on the highest quality site-type modulated their courtship intensity to female quality (i.e., female size). This indicates that males required some minimal level of resource attractiveness (i.e., a threshold) before they exhibited mate preferences based on female quality. Further differences in the resource attractiveness for males defending the high-quality artificial sites were not related to differences in courtship behavior.
Key words: beaugregory damselfish, courtship, habitat quality, mate choice, Stegastes leucostictus.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Most models of mate choice consider females and rely on the common observation that females first assess a number of available males before selecting a mate (e.g., Andersson, 1982
; Dugatkin,
1992; Moller and Pomiankowski,
1993; Real, 1991;
Sullivan, 1994). The number of
males assessed before mating is expected to be influenced by the costs and
benefits of continuing to search for the best male (e.g.,
Sullivan, 1994). A common
assumption of many of these models is that males are equally receptive to all
females (see review by Reid and Stamps,
1997).
Although few reports exist of males rejecting females, experiments reveal
that males, when presented with a choice, exhibit mate preferences and
typically spend more time courting the more fecund (e.g., larger) female
(Olsson, 1983;
Sargent et al., 1986;
Verrel, 1982). For males,
courtship may be costly (e.g., susceptibility to predators;
Endler, 1987;
Forsgren, 1992), which has been
used to explain the preference for more fecund females. That is, males risk
more courtship when the payoff (i.e., number of offspring) is higher.
Although empirical evidence illustrates a seemingly simple preferential
system based on female quality, the measurement of male preference is
complicated by male attractiveness. This complication is especially apparent
in polygynous species where males must wait for females to approach them
before exhibiting their own preference. Few empirical or theoretical studies
have considered how changes in a male's attractiveness may influence his mate
preference. Real (1991)
predicted complex interactions; for example, the presence of highly attractive
and selective females may cause highly attractive males to become
correspondingly selective.
Here we examined how changes in male resource attractiveness influence male
mate preferences in the territorial beaugregory damselfish (Stegastes
leucostictus). Because beaugregory males modulate their courtship
intensity based on female size and do not typically reject females
(Itzkowitz et al., 1998), we
considered two aspects of male courtship that have been linked to male
attractiveness: overall courtship intensity and the modulation of courtship
intensity with female quality ("selectivity"). Reynolds
(1993), while not commenting
on male preferences, observed that courtship intensity may be either
positively or negatively correlated with male attractiveness. The type of
correlation resulted from a host of potentially complex relationships between
courtship costs and benefits. As mentioned above, Real
(1991) did consider male
selectivity by illustrating how male attractiveness may develop mate
selectivity.
Male beaugregory preferences may be described by one of the mate choice
models proposed for females. Reid and Stamps
(1997) reviewed a number of
these models and observed that they fell into two general categories: the
comparison model and the threshold model. The comparison model predicts that
females will select the best male from among a group of available males. The
threshold model predicts that females select any male that has a quality above
a threshold level.
To apply the comparison model to male beaugregories, we predicted that they would base their preference (i.e., expressed by their courtship intensity and/or selectivity) on the relative quality of their own resource. This requires that they compare the quality of their resource with those of their neighbors. Any quantitative differences in the relative quality of a male's resource will be translated into quantitative changes in his overall courtship intensity and/or selectivity. The threshold model, when applied to beaugregory males, predicts that males require some level of resource quality before modulating their courtship costs and/or selectivity. Any further quantitative differences in the resources above the threshold will have no impact on male courtship.
Our first objective was to detect whether the quality of the male
beaugregory's resource influenced his courtship intensity, irrespective of
female size. We tested this prediction by comparing the courtship of males
that used different quality habitats while controlling for female size. If
habitat quality did influence male courtship intensity, we then intended to
examine how resource quality might influence a male's courtship intensities to
females of different qualities. That is, did males with more attractive
resources more carefully modulate their courtship to female size than males
with less attractive resources? This extended a previous study that showed
that males intensified their courtship to larger females
(Itzkowitz et al., 1998). If
resource attractiveness did influence male courtship, our next objective was
to test the applicability of the resource comparison and threshold models.
Finally, if males exhibited the threshold effect, we wanted to determine if a
plateau in male courtship behavior existed as predicted by the threshold
model. We manipulated the attractiveness of the male's territory (as defined
by the amount of eggs he received) by using both natural and artificial
breeding sites (see Itzkowitz,
1991; Itzkowitz and Makie,
1986; Itzkowitz et al.,
1995). We tested male courtship by presenting males with
different-sized females housed in a clear jar.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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The beaugregory damselfish inhabits the quiet, shallow lagoons behind the reef crests in the Caribbean. In Jamaica, males defend permanent all-purpose territories around pieces of rubble that serve as egg deposition sites (Itzkowitz, 1977
). Females
arrive alone at the male's territory. When a female nears the male's
territory, he moves toward her while performing the dip display, rapidly
swimming forward and down for several centimeters, and then quickly ending
with an upward jump of several centimeters, during which the dorsum becomes
bright yellow. The dip occurs only during courtship. Receptive females enter
the male's territory, deposit adhesive eggs within a crevice, and depart. The
male provides no direct parental care, but his territorial defense does
protect the eggs from diurnal egg predators such as the blue head wrasse
(Thalassoma bifasciatum) and other conspecifics
(Itzkowitz and Makie, 1986).
Several females may deposit their eggs in the same territory.
A male's reproductive success depends on the structure of his breeding
site. Males given new artificial sites have a much higher reproductive success
than males on natural sites (Itzkowitz,
1991; Itzkowitz et al.,
1995), although the attractiveness to female of artificial sites
in place for long periods (e.g., > 6 months) declines. Furthermore, males
on older artificial sites show a dramatic improvement in their reproductive
success upon exchanging their old site for a new one
(Itzkowitz et al., 1995). This
improvement is not based on changes in the space available for additional egg
clutches because both old or new sites have an abundance of space, and past
studies have shown that it is extremely rare for any site to be fully occupied
by eggs (Itzkowitz, 1991). The
decline in the quality of the artificial sites seems related to eventual
presence of egg predators such as brittlestars
(Itzkowitz and Koch,
1991).
Test subjects
The study was conducted in the backreef habitat in Discovery Bay, Jamaica,
during a 3-week period in July/August 1996. Three different classes of males
served as subjects: (1) males on new sites, (2) males on old artificial sites,
and (3) males on natural sites. We randomly selected 28 males defending
natural rubble sites, and each male had a cleaned artificial site placed
within its territory. These sites were designated as "new," and
previous studies have described the structure of these breeding sites as
"five-entry sites" (Itzkowitz,
1991). The structure of these sites consisted of four tubes of PVC
pipe bolted into a "+" pattern on a 30-cm2 plastic
base. Each tube was 10 cm long with a 7 cm diameter
(Figure 1). Females deposited
their adhesive eggs on the inner upper side of a tube. Entry into a tube was
through the exterior entrance or, at other end, through the upper space where
the four tubes met in the center.
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"Old" sites were structurally identical to the "new" sites but had been placed in the water at least 12 months before the current study. We randomly selected 28 old sites from a larger group and allocated them to males dispersed among those males given "new" sites. Finally, males defending "natural sites" were randomly selected in the same general area as the "new" and "old" artificial sites.
Females were captured in an adjacent area and were all individuals that had been naturally courted by males. These fish were often used immediately for testing or taken to the laboratory where they were maintained in a flow-through seawater tank for several days. Both types of females seemed to exhibit the same behavior of swimming continuously along the walls of the bottle for the entire testing period. We measured the standard length of each female immediately before testing and released each back into its initial habitat after testing.
Male mating preferences
One female was placed in a 2-1 plastic jar ("Nalgene") and
placed approximately 10 cm from the edge of the male's breeding site, who
typically approached the female within seconds after the jar was positioned.
Male courtship was quantified as the number of swimming dips he performed
during the 3-min observation. We observed the resident male for 3 min after he
first approached the jar. We used the 3-min period because it allows males
sufficient time to respond to the female and is short enough to allow us to
test sufficient numbers of males. At the end of the 3 min, the jar was moved
to the next male.
We tested males only once with a specific female. However, the same female was typically tested with 12-14 males in succession. Each male was tested only once during a day. Each male on new artificial sites was tested with an average of seven different females during the 3 weeks of this study. Similarly, males using either an old artificial or natural sites were presented with an average of six and four different females, respectively. In all, we used 14 different females on new artificial sites, 12 on old artificial, and 8 on natural breeding sites.
Male reproductive success
Reproduction could be measured only for the 28 males on new sites because
males defending old and natural sites rarely mate
(Itzkowitz, 1991;
Itzkowitz et al., 1995).
Reproductive success was measured by the area occupied by the eggs within the
breeding site. The egg mass was ovoid in shape, and its length and width was
estimated, and then the product was used as a relative measure. We placed eggs
in one of three categories based on an estimate of their age: (1) new eggs,
deposited within the previous 24 h, were bright yellow, (2) final eggs are
black/dark purple and were expected to hatch within the next 24 h; and (3)
eggs older than "new" eggs but younger than "final"
eggs were called "intermediate." The entire egg stage typically
lasted about 6 days. Reproductive data were collected every morning during the
3 weeks of this study.
Statistics
All statistical tests were performed using the Statgraphics program. All
data were normally distributed, and two-tailed tests were performed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Male courtship intensity and site quality
A total of 14, 12, and 8 females were presented to males using the new, old, and natural sites, respectively. From these presentations, we selected those in which similar-sized females were presented to all three male groups on the same day. We had seven such replicates ("blocks"). Although the size of females differed widely between these blocks, the differences among females within a block was less than 1 mm. A group mean dip rate was generated for each female (i.e., total number of dips generated by all males in a group to whom she was presented/number of males) and termed the "group mean dip rate." Using a one-way blocking design that controlled for female size, the mean dip rate was significantly different among the male groups using the three breeding sites (F2,12 = 7.64, p =.0072; Figure 2). The multiple range test indicated that group mean dip rates were higher for males on new artificial sites than for those on old artificial and natural sites (p <.05), but not different between males on old artificial and natural sites (p >.05). We also considered all female presentations using a one-way ANOVA because the size distributions of females presented to the three groups were closely matched (i.e., similar means, variances, and ranges), and here also the mean dip rates were significantly different (F2,32 = 5.9, p <.02).
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Courtship intensity, habitat quality, and female size
For males using new artificial sites, a highly significant positive
correlation existed between female size and the group mean dip rate
(n = 14 females, r =.73, p <.001;
Figure 3a). Five other females,
each less than 60 mm long, were presented to these males as part of a
different experiment. Males generated very low courtship intensities to these
females, and when these are included, the correlation between female size and
group mean dip rate increases (n = 19, r =.87, p
<.001). Courtship intensity (i.e., group mean dip rate) was not
significantly correlated with female size for males on old artificial sites
(n = 12 females; r =.28; p >.05;
Figure 3b) or males on natural
sites (n = 8 females; r =.12; p >.05;
Figure 3c). Thus, only males on
new artificial sites modulated their courtship intensity (i.e., dip rate) in
response to female size.
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Courtship intensity and male reproductive success
The following analyses apply only to males using new artificial sites
because reproduction could not be monitored for males on old artificial and
natural sites (see Materials and Methods). Each male on a new artificial site
was presented with an average of seven females. By averaging the dip rates
each male performed for all females presented to him, we generated a male's
mean dip rate (i.e., total number of dips generated by a male to all
females/total number of females presented to the male). A male's mean dip rate
was not significantly correlated with the total amount of new eggs the male
received during the study (N = 28; r = -.046; p
>.05). Similarly, the male's mean dip rate was not significantly correlated
with the total amount of final eggs (those that will hatch within 24 h;
N = 28; r = -.09; p >.05). Thus, relative
reproductive success was not related to courtship intensity.
To determine the relationship between a male's selectivity and his reproductive success, a correlation (r) was generated for each male between dip rate and the corresponding female size. We considered this correlation an index of the degree to which a male modulated his courtship intensity to female size. Given the small number of females presented to each male (about seven), this index must be viewed with caution. Considerable variation existed in the indexes among males (range = -.473 to.897; x = 0.467 ± 0.06) and was not significantly different from a normal distribution (Kolmogorov test; D = 0.143, p >.60). The index was not significantly correlated with the total amount of new eggs received by each male (r =.167; p > 0.05; N = 28 males). We also considered the possibility that only the most successful males (i.e., the top 10 males) were modulating their courtship with female quality. Here also, we found no significant correlation (N = 10, r =.24, p >.05). Nor were those males with the highest indices (i.e., most careful in modulating their courtship to female quality) the most successful males (N = 10; r = -.19, p >.05).
Courtship intensity and the presence of eggs
We compared the courtship intensity of males on new artificial sites with
the amount of new, final, and total eggs (includes new, intermediate, and
final eggs) present at the time of the test. We did not compare males across
different days because we used different-sized females. Instead, we examined
whether, within a subgroup of males on a specific date, the courtship was
significantly correlated with the amount and/or types of eggs present. We did
not use tests before July 31 because insufficient amounts of eggs were present
to perform the correlation test. No significant correlations were found for
courtship intensity with the amount of new eggs, the amount of final eggs, or
the total amount of eggs in all stages (i.e., new, final, and intermediate
eggs) present at the time of the test
(Table 1). Also, as shown in
Table 1, female size did not
appear to influence whether males modulated their courtship based on the
amount or types of eggs present. Nor did we find any significant correlations
between the amount of eggs the day before or the day after the dipping rate
test was performed.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Males with unattractive resources showed lower courtship to all females, and their low courtship intensity was independent of female fecundity. In contrast, the males with experimentally attractive resources heightened and modulated their courtship intensity to female fecundity. Real (1991
) suggested that males
with fewer opportunities to mate would be less selective, and this may explain
why beaugregory males on poor-quality breeding sites treated all females
similarly.
Courtship intensity
The higher courtship levels of males with attractive resources seem
counterintuitive given that such males may have little need to invest in
courtship. Furthermore, the cost for intense courtship may be quite high
because the only successful predatory attempts during the bottled female tests
were on males using high-quality, new artificial sites (Itzkowitz, personal
observation). Other studies have shown that the presence of predators reduces
courtship intensity (e.g., Endler,
1988; Forsgren and Magnhagen,
1993). Perhaps the beaugregory males used their courtship
intensity to advertise the quality of their sites. Because females eventually
inspect the breeding site, males on poor-quality sites cannot gain from being
dishonest advertisers. For these males, the best strategy might be for them to
reduce courtship costs and wait for high-quality sites to appear after the
numerous storms that rearrange the rubble habitat
(Itzkowitz et al., 1995).
The differences in courtship intensity among males defending the different qualities of sites were quantitative, rather than qualitative (i.e., present/absent), and are more suggestive of the comparison model than the threshold model. It is possible that the responses by males on poor-quality breeding sites resulted from an experimental artifact. Perhaps by placing the bottled females close to the breeding sites we simulated females that were about to mate with these males. Thus, even males with less attractive resources might have been stimulated to court. More recent preliminary tests that placed females at greater distances from the breeding site more strongly support the threshold effect.
Courtship selectivity
Our selectivity measures did support the threshold model. Male selectivity,
as seen by the significant correlation between female quality and courtship
intensity, occurred only on the high-quality breeding sites. Thus, males with
more attractive resources were more selective in their mate preferences.
However, selectivity among these males was highly variable, suggesting that if
a plateau effect did exist (i.e., all males exhibiting the same degree of
selectivity), it was not based on the type of breeding site.
Intensity and selectivity above the threshold
The large reproductive differences among males on new artificial breeding
sites (see Itzkowitz, 1991;
Itzkowitz et al., 1995)
suggests that other features influenced male attractiveness (perhaps
microlocation or the males' inherent quality). These differences did not
appear to have any additional effect on courtship intensity or selectivity.
More proximate differences, such as the presence and/or quantity of eggs,
although enhancing a male's ability to attract more females (e.g.,
Dugatkin, 1992;
Itzkowitz and Makie, 1986;
Knapp et al., 1995), also were
not significantly correlated with his courtship intensity.
Possibly, males were unable to further assess their relative quality, or the quality of their resources, to fine tune their selectivity. For example, to assess the exact degree of a neighbor's attractiveness would require consistent and frequent access into the neighbor's breeding site. The rigorous territorial defense by beaugregory males may make it difficult to make such invasions. Consequently, they may have relied on the gross quality of their breeding to estimate their attractiveness to females, and the variable degrees of selectivity among males may result from the incomplete information each male had about his neighbor's success.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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We thank J. Smith, J. Homes, and L. E. Schroeder for their field assistance. M. Richter provided important statistical help R. Macias-Ordonez, J. Nyby, L. Schroeder, and two anonymous reviewers provided many helpful comments on the manuscript. This is Discovery Bay Marine Lab publication 614.
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