Behavioral Ecology Vol. 13 No. 3: 366-374
© 2002 International Society for Behavioral Ecology
Sexual selection for structure building by courting male fiddler crabs: an experimental study of behavioral mechanisms
a Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Ancón, República de Panamá, or Unit 0948, APO AA 34003, USA b Department of Marine Biological Science, Faculty of Fisheries, Hokkaido University, Hakodate 041-8611, Japan
Address correspondence to J.H. Christy, Smithsonian Tropical Research Institute, Unit 0948, APO AA 34002, USA. E-mail: christyj{at}naos.si.edu . P.R.Y. Backwell is now at the Division of Botany and Zoology, The Australian National University, Canberra ACT 0200, Australia.
Received 12 October 2000; revised 25 June 2001; accepted 31 July 2001.
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ABSTRACT |
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Males of the fiddler crab Uca musica sometimes build sand hoods at the entrances of their burrows, to which they attract females for mating with claw waving and other displays. Females significantly more often approached males with hoods than males without hoods, but once at a burrow, they were just as likely to stay and mate whether the male had a hood or not. To determine how hoods affect male attractiveness, we conducted experiments that controlled for other differences in courtship behavior between builders and nonbuilders; we removed hood builders' hoods and we added hood models to nonbuilders' burrows. We then measured the attractiveness of hood builders and nonbuilders with and without hoods. Neither manipulation measurably affected male courtship behavior. The presence of a hood did not increase male—female encounter rates, suggesting that hoods do not attract distant females into a male's courtship range. However, once a male courted a female, she was significantly more likely to approach if he had a real or model hood. We obtained direct evidence that females orient to hoods by replacing them with hood models positioned about 3 cm away from the openings to males' burrows. Females approached the models, not the courting males, about 27% of the time. We conclude that hood building is sexually selected because courted females differentially approach hoods, not because hoods attract distant females and not because females prefer to mate with hood builders.
Key words: behavioral mechanisms, bowers, courtship, female preferences, fiddler crabs, male-built ornaments, sexual selection, Uca musica.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Sexual selection by female responses to male courtship signals and displays has been implicated in the evolution of diverse male characters that mediate sexual communication at all scales (Andersson, 1994
;
Darwin, 1871). Experimental
studies in which male traits are manipulated are perhaps most convincing
(Wilkinson et al., 1987)
because they can provide direct evidence that a trait is sexually selected by
a female response to its presence, form, or degree of development.
Courting male Uca musica build sand hoods at the entrances of
their burrows, to which they attract females for mating (Zucker,
1974,
1981). In addition to U.
musica, males of 16 of the nearly 100 species in the genus
(Rosenberg, 2000) build mud or
sand hoods, pillars, semi-domes, lips, or rims at their burrows (14 species
listed in Christy [1988a] plus
U. perplexa [Christy, unpublished data], U. crenulata
[deRivera CE, personal communication], and U. annulipes [Backwell,
unpublished data]). Like the bowerbirds' bowers
(Gilliard, 1969), the display
courts of some other birds (Andersson,
1991), and the sand structures built by some cichlid fish
(McKaye et al., 1990) and
other ocypodid crabs (Jones,
1972; Linsenmair,
1967), fiddler crab structures are "external
ornaments" (Andersson,
1991), constructions that exist physically apart from their
builders. Unlike male-built nests, hoods are not used during breeding, and
they have no utility to either sex beyond their possible role in courtship.
The objective of this study was to determine experimentally how hood building
by males of the fiddler crab U. musica might be sexually selected by
a differential female response to hoods.
Reproductive behavior of Uca musica
Uca musica (about 1 cm adult carapace width) lives in mixed-sex
colonies on intertidal sand flats and bars in estuaries and bays in the
tropical Eastern Pacific, where it breeds year-round
(Crane, 1975). Except when
mating, crabs occupy burrows alone. Crabs are inactive at night and for 2-3
consecutive days of each biweekly tidal amplitude cycle when low tides occur
near dusk and dawn. Consequently, hood building, courtship, and mating follow
a biweekly cycle (Zucker,
1976,
1978). Males court from and
defend burrows in the middle to upper intertidal zones
(Zucker, 1984). Those that
court vigorously build hoods and usually blanch to cream or brilliant white,
except for bluish wash on the outer lower surface of their single large
cheliped. All males probably are hood builders, but they do not blanch and
build hoods every day (Christy et al.,
2001).
To choose mates, females leave their burrows and move through the area with
males who court them with lateral-circular claw waving. Waving males either
stay close (typically 
15 cm) to their burrows and move but a few steps
back to them when females approach, or they range up to about 1 m from their
burrows, approach females closely ( 5 cm), switch to rapid vertical
waving, and lead them back to their burrows. Females sequentially stop at
several males' burrows before they stay in one
(Zucker, 1984), and they
rarely return to a male after visiting another. Mate choice is indicated when
a female stays in a male's burrow and he plugs the entrance and upper shaft
with sand. The pair copulates in the burrow, and about 2 days later
(n = 43) the female produces a clutch of eggs, which she carries
attached to her abdominal appendages. The male then digs an emergence shaft
and leaves the female to incubate in the burrow.
Effects of hoods on courtship
Hoods might increase male courtship success by increasing the rate
(frequency) that (1) males encounter and court females, (2) courted females
approach males and their burrows, and (3) females mate with the males they
approach (Andersson [1989,
1991] and Borgia
[1995] discuss the sequential
effects of avian display ornaments). Hoods may increase encounter rates in two
ways. Fiddler crabs see two-dimensional objects on the surface poorly, and
they do not use vision to locate their burrows entrances if they are more than
a few centimeters away (Zeil,
1998; Zeil and Layne,
2002). In contrast, they see vertical objects such as hoods, which
are as tall as or taller than their eyestalks, exceptionally well
(Land and Layne, 1995;
Zeil and Al-Mutairi, 1996).
With a hood marking his burrow, a male may safely range farther from it and
increase the rate at which he intercepts females. Hoods also should be
conspicuous to distant females (Figure
1b). As they move between males' burrows, females may
preferentially orient to hoods. This response also would increase the rate
that hood builders encounter and court females. Similarly, once a male has
directed claw waving to a female, she may be more likely to approach if his
burrow is marked with a hood (Christy,
1988b; Crane,
1975; von Hagen,
1968). Finally, hoods may signal either male or burrow quality
(Backwell and Passmore, 1996;
Backwell et al., 1995; Christy,
1983,
1987) and increase the
probability that a female will mate with a male once she reaches his burrow.
Thus, hood builders may have higher mating rates because they are more likely
to encounter and court females, to attract the females they court, and to mate
with the females that they attract.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We conducted this study in February—April, September, and November 1995, March—May 1998, and January—June 1999. We observed crabs at various locations on shifting sand bars and flats on the west bank of the Pacific entrance to the Panama Canal about 1 km upstream of the Bridge of the Americas. Data for experimental contrasts were taken at the same locations on the same days.
Male courtship success
Male mating rate (frequency) should be the product of the three rates
discussed above. We measured the rate that courted females approached males,
step 2, and the rate that females mated with the males they approached, step
3. However, we could not reliably determine when a male missed a courtship
opportunity so we could not accurately measure male success at step 1. We
therefore took an indirect approach and measured the rate that females visited
males with and without hoods. Visitation rates are the product of encounter
(step 1) and approach (step 2) rates. We used independent measurements of
approach rates to determine whether hoods affected encounter rates.
Hood removal and addition experiments
We did two kinds of experiments to control for the possible effects of
behavioral differences between hood builders and nonbuilders on male courtship
success. We removed the hoods of hood builders, and we added hood models to
the burrows of nonbuilders and compared the courtship success of these males
to that of hood builders with their hoods present and nonbuilders without
hoods. A convenient feature of male behavior facilitated the removal
experiments. Beginning about 1 h after low tide, when many females are
searching for mates, hood builders rarely rebuild their hoods if they are
damaged. We therefore created hoodless hood builders by removing their hoods
at 1-1.5 h after low tide. For the hood addition experiments, we made replicas
of a hood from a latex mold of a real hood. The hood we replicated was nearly
symmetrical, and its height (23 mm) and width (33 mm) were within 1 mm of the
average hood (n = 100). We glued sand from the study area on the
replicas so that they looked to us like real hoods
(Figure 1c). We observed crab
courtship behavior and measured male success under eight experimental and
natural conditions. For clarity, we describe the methods, analysis, and
results for each separately below.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Attractiveness and mating rates
To determine if hood builders more often attract mates than do nonbuilders, we recorded the responses of individual females to courting males. We watched both receptive and unreceptive females. Receptive females stayed in males' burrows, which the males then plugged. We assume that these pairs mated. Unreceptive females occupied empty burrows or ones from which they displaced the residents. Some of these unreceptive females may have been searching for mates but did not find them. We recorded when we first and last saw each female, whether she approached or passed each male who courted her, whether each male had a hood, and whether she stayed in the male's burrow. From 2 to 46 males courted each female. Using a two-way ANOVA for paired comparisons (Sokal and Rohlf, 1995
), we
asked whether individual females differentially approached hood builders
compared to non-builders and whether there was significant variation among
females. We considered only females who where courted by at least five males
of each class. The response variables were the arcsines of the square roots of
the proportions of approaches by each female to builders and nonbuilders. We
also asked whether hood builders were differentially attractive to females
generally, as expected if there is sexual selection for hood building.
Individual females contributed several observations to the total, but only one
per courtship and male, so we treated each response as a statistically
independent observation (see also
Andersson, 1989). We used
G tests of independence (with William's correction;
Sokal and Rohlf, 1995) to
determine whether hood builders were more attractive percourtship (step 2),
whether they were equally attractive to receptive and unreceptive females, and
whether, after being attracted to a burrow, receptive females preferred to
mate with builders (step 3). We watched 28 receptive females for 17.4 ± 17.95 min (mean ± SD; range: 2-70 min) until they chose mates and we recorded their responses to 17.5 ± 13.67 males (2-46). We watched 34 unreceptive females for 17.3 ± 12.89 min (2-44 min), and we recorded their responses to 8.9 ± 8.71 males (1-41), about half the mean number that courted receptive females in the same average time. Because we started watching females after they began searching, these values underestimate the true means.
Receptive females (n = 12) who were courted by at least five
builders and five nonbuilders were significantly (F1,11 =
14.404, p <.005) more attracted to builders (mean approach rate:
to builders = 0.823; to nonbuilders = 0.642). There was no significant
variation among receptive females (F1,11 = 1.646,
p >.10) in approach rates, but the power of this test to detect
even a medium effect was low at 21%
(Buchner et al., 1997;
Faul and Erdfelder, 1992).
Unreceptive females received too few courtships for this analysis.
Hood builders were more attractive than were nonbuilders and equally so to
receptive and unreceptive females. Nonbuilders also attracted both classes of
females at the same frequency (Tables
1 and
2). The presence of a hood did
not significantly affect the frequency that females stayed at males' burrows
to mate (Table 2). Sample sizes
for these tests were sufficient (254) to give a power of > 99% to
detect a small effect (Cohen,
1988). Hence, builders were differentially attractive, but we
found no evidence that females subsequently preferred to mate with them.
Multiplying these rates gives 0.07 matings/courtship for hood builders, about
40% greater than the nonbuilder rate of 0.05 matings/courtship.
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The result that hoods do not affect mating decisions after females approach
males' burrows appears to be robust. During a hood addition experiment
(described below), we recorded a median rate of 0.4286 visits/h to builders
with natural hoods (n = 36). In another study
(Christy et al., 2001),
hood-builder mating rates averaged 0.09 matings/day (n = 27 days,
> 150 males/day) and varied little with hood abundance. We estimate that
these males received 1.072 visits/day (0.4286 visits/h x 2.5 h
courting/day), giving 0.084 matings/visit (0.09 matings/day ÷ 1.072
visits/day), closely comparable to the estimate of 0.085 matings/visit we
obtained from following individual females
(Table 2).
Behavior of hood builders and nonbuilders
Behavioral differences other than hood building between builders and
nonbuilders may contribute to differences in their attractiveness. On 3 days
we used scan sampling at 5-min intervals to record male behavior with respect
to seven activities: feed, wave-feed (waving while feeding), wave, threaten
(includes threat-feed, a rare activity), fight, in burrow, and other (includes
self-maintenance). We observed males for 3 h from 1 h before to 2 h after low
tide. At low tide we noted whether each built a hood and his degree of
lightening (dark, medium, white). We expected
(Christy, 1988b) that hood
builders would court more and feed less than nonbuilders. We used one-tailed
Mann-Whitney U tests (Sokal and
Rohlf, 1995) to compare the courtship frequencies (wave +
wave-feed) of the two classes of males, with each male contributing a single
frequency value. We compared the frequency of aggression (threat + threat-feed
+ fight) between builders and nonbuilders with a two-tailed test because we
could not predict the direction of the difference. We used a G test
to determine if hood building and body brightness are associated, and we
examined the value of Somer's d, which measures the strength and
direction of association between ordinal variables in rectangular tables (+1
to -1; Wilkinson et al.,
1996).
Builders (n = 37) and nonbuilders (n = 75) spent about the same relative amount of time feeding and courting (Figure 2), but they distributed their time differently between these activities. Hood builders fed significantly less (U = 2130.5, p <.001; one-tailed), and they courted significantly more (U = 1086.5, p <.031; one tailed), spending nearly half (47.4%) their time waving without feeding. Both classes of males spent little time on aggression (4.7%). Male brightness and hood building were significantly positively associated (Gw = 6.476, p <.05; Somer's d = 0.245 ± 0.097, p <.01); 62% (23/37) of hood builders but only 43% (33/77) of nonbuilders blanched to white at low tide. These behavioral and color differences could contribute to the greater attractiveness of hood builders.
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Effects of hood removal on hood builder behavior
The effects of hoods on attractiveness can be inferred directly from the
hood removal experiments only if this manipulation does not affect
attractiveness by changing male courtship behavior. On 5 days we marked the
burrows of 18-36 hood builders. Beginning at low tide, we used scan sampling
to record their behavior with respect to the activities listed previously. At
1.5 h after low tide we removed the hoods from every other burrow and resumed
observing for another 1.5 h. We used a one-tailed Mann-Whitney U test
to determine whether males, half of whom had their hoods removed, courted less
after the manipulation.
Hood removal had no significant effect on male courtship or aggressive
behavior. Before we removed hoods, males in both groups spent about the same
amount of time courting (78.9%, hoods later removed; 78.1%, hoods left on).
After we removed hoods, males in both groups waved less and wave-fed more
(Figure 3), giving an overall
slight decline in courtship (74.7%, hoods removed; 74.5%, hoods left on).
There was no significant difference between the two groups in the reduction in
percentage of time waving (U = 2459.5, p =.422) or in the
increase in percentage of time wave-feeding (U = 2675.5, p
=.079), with a power of 82% for each test to detect a medium effect
(Buchner et al., 1997;
Faul and Erdfelder, 1992).
Rates of aggression were low, and they decreased slightly for both groups
after we removed hoods (Figure
3).
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Effects of hood removal on attractiveness
On 7 days, we marked 80-200 hooded burrows by placing a small stick about
15 cm from each one. At 1 h after low tide we removed the hoods from every
second burrow, creating an approximately even spatial distribution of builders
with and without hoods. Nonbuilders also were present throughout. We watched
individual females for several courtships but usually not until they chose
mates. We recorded whether the female passed or approached each male who
courted her and the status of the male. We used G tests of
independence to determine if approach frequencies depended on male status.
Builders with their hoods were significantly more attractive than were builders without their hoods, who in turn were significantly more attractive than nonbuilders (Table 3). The first difference indicates that hoods directly affect attractiveness. The second difference suggests that frequent waving and a light color also contribute to male attractiveness.
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Effects of hood removal on visitation and encounter rates
On 9 days we marked 50-120 burrows with hoods. At about 1 h after low tide
we removed every second hood, creating an approximately even spatial
distribution of builders with and without hoods. For the next 1.5-2 h we
recorded each time we saw a female visit a male at a marked burrow and whether
he had a hood. We watched a given female for only a few visits, and then
shifted our attention to another. We tallied visits at 10-min intervals and
noted when any male mated, left, or was ousted from his burrow or
disappeared.
The distributions of visitation rates (visits/h) to both groups of males
were bimodal, as many males were never visited. We used a G test of
independence to determine whether visit frequencies of 0 or 
1 depended on
male status. The distributions of visitation frequencies 1 were strongly
skewed to the right. We therefore compared the median (rather than the mean)
visitation rates between the two groups of males (Fisher's Exact test;
Sokal and Rohlf, 1995).
We saw 807 visits to 460 builders with and 378 builders without hoods.
Eliminating 45 males that we saw for less than 30 min, builders with hoods
were significantly (GW = 12.481, p <.001) more
likely be visited at least once (56.8%, 252/444) than were builders without
hoods (44.1%, 154/349). Considering males who received 1 visit, the
median rates were 0.923 visits/h to males with hoods and 0.754 visits/h, to
males without hoods, a nonsignificant difference (Fisher's Exact test,
p =.457, tails; n = 377, power > 99% to detect a small
effect).
Shifting the analysis from individual visitation rates to the sample of
visits, we used G tests of goodness-of-fit
(Sokal and Rohlf, 1995) to
test two hypotheses. First, we asked whether the relative proportions of
visits to builders with and without hoods differed from those expected based
on the relative amount of time males in the two groups courted weighted by the
relative proportions of visits when they courted. For each group we calculated
the sum, across males, of the number of minutes each was active during each
10-min observation period. We then multiplied these sums by the proportions of
the 807 visits that we observed during each of the periods and summed these
values across periods. These group sums, each divided by the grand sum for the
two groups, gave the expected proportions of visits to each group under the
null hypothesis of equal visitation rates. The observed frequencies of visits
to the two groups did not fit the expected frequencies (GW
= 13.432, p <.001). Hood builders with hoods were visited more
often (observed — expected: 518-467 = 51), and those without hoods were
visited less often (289-340 = -51) than expected.
Second, we tested the hypothesis that there was no difference between the
relative proportions of visits to the two male groups and those expected based
on their relative attractiveness per courtship (step 2). If we fail to reject
this hypothesis, then we have no evidence that builders with hoods received
disproportionately more visits because they encountered and courted more
females (step 1). The expected frequencies for this test were calculated from
the products of the expected frequencies in the previous test and the relative
frequencies that courted females approached builders with and without hoods
(Table 3). Dividing each of
these values by their sum gave the expected relative proportions of visits to
the two groups. There was no significant difference between the observed and
expected frequencies of visits (GW = 0.441, p
>.50; observed — expected; hood present: 518-527 = -9; hood removed:
289-280 = 9; power > 80 % to detect even a 0.05 difference in relative
frequencies relative to the null expectations;
Cohen, 1988). Hoods did not
enhance male—female encounter rates.
Effects of hood addition on attractiveness
On 9 days we marked the burrows of 20-30 builders and non-builders that
were approximately evenly distributed across the observation area. Just before
low tide, we removed builders' hoods and replaced them with model hoods, and
we added models to the burrows of neighboring nonbuilders. This manipulation
produced four spatially intermixed groups of males: builders with natural and
model hoods and nonbuilders with and without model hoods. We watched
individual females for a few courtships and recorded whether they passed or
approached each male who courted them and the male's group membership.
There was a significant difference in attractiveness among males in the four groups. Nonbuilders without hoods were relatively unattractive compared to males with hoods, who did not differ greatly in attractiveness (Table 4; power > 99% to detect a small effect in all nonsignificant tests). The presence of a hood increased male attractiveness. Unlike the results of the hood removal experiment, the more frequent waving and the brighter color of builders did not.
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Effects of hood addition on visitation and encounter rates
Using hood removal, we found no evidence that hoods increased the rate that
males encountered and courted females. We therefore predicted that the
addition of hood models to nonbuilders' burrows also would not increase these
rates. On 5 days, beginning at about 30 min before low tide, we marked 60
builders' and nonbuilders' burrows. The manipulation described above was done
creating the same four groups of spatially intermixed males. For the next
2-2.5 h, we recorded and tallied at 10 min intervals each time we saw a female
visit a male and whether the male had a natural or model hood. We noted any
change in male status. The analysis followed the procedures described above,
except we used a G test to compare median visitation rates between
the four classes of males (Sokal and
Rohlf, 1995).
We saw 836 visits to 529 males: 130 nonbuilders, 128 nonbuilders with model hoods, 136 builders with natural hoods, and 135 builders with model hoods. Eliminating four males that we watched for < 30 min, whether a male received at least one visit did not depend on his group membership (GW = 4.2448, p >.10, n = 525, power > 99% to detect a small effect). For males that received at least one visit, the median rates (visits/h) were 0.429 to nonbuilders without hoods, 0.800 to nonbuilders with model hoods, 0.775 to builders with natural hoods, and 0.857 to builders with model hoods. These medians were not significantly different (GW = 2.657, p >.10; n = 353, power > 99% to detect a medium effect).
There was a marginally significant difference between the observed and expected frequencies of visits to these four groups of males (GW = 7.859, p =.049; observed — expected; nonbuilders: 176-207 = -31; nonbuilders with models: 201- 203 = -2; builders with natural hoods: 219-210 = 9; builders with models: 240-216 = 24). Nonbuilders without hood models received substantially fewer visits and builders with models received substantially more visits than expected. However, the observed frequencies of visits to the four groups differed significantly in the direction opposite that expected from their differential attractiveness and their availability for visits. Nonbuilders without hoods received more visits and builders with model hoods fewer visits than expected (GW = 15.083, p <.01; observed — expected; nonbuilders: 176-135 = 41; nonbuilders with models: 201-207 = -6; builders with natural hoods: 219-224 = -5; builders with models: 240-270 = -30). Hoods reduced the rates at which males encountered and courted females.
Orientation to displaced model hoods
Our hood manipulations may have changed male behavior in some unknown way
that affected attractiveness. To obtain direct evidence that courted females
approach hoods, we did an experiment in which females could approach either
the courting male as he entered his burrow or his hood. On 8 days, beginning
at about 1.5 h after low tide, we removed hoods from 54 burrows and replaced
them with models, each facing in the direction of the hood it replaced. Each
model was positioned so its center was about 3 cm to one side of the burrow
and its nearest edge was about 0.5 cm away from the opening
(Figure 1d). Provided that
courting males return to their burrows and not the models, this manipulation
would spatially separate orientation cues from the male and hood. We placed
models on alternate sides of the burrows on successive days. We watched
individual females for one to a few courtships. For each that resulted in an
approach, we recorded whether the male came close to the female and then led
her to his burrow, whether the female and male ended their approach at the
burrow opening or the model hood, and whether the female approached from the
90° sector (estimated by eye) in front, in back, on the side with, or on
the side without the model.
Females approached model hoods about 27% of the time (Table 5). Where they stopped depended on the direction from which they approached. Females that approached from the side with the hood usually (25/32, 78%) stopped at the hood, and those that approached from the side with the burrow opening usually (71/75, 95%) stopped at the opening (GW = 58.781, p <.001). Because they approached from the side, these females must have seen hoods and males in near alignment. They often stopped at the object they encountered first, making it uncertain to which of the nearly aligned objects they were orienting. Females that approached from the front and back sectors should have seen hoods and males at greater angular separations. Where these females stopped depended on whether males closely led them to their burrows (GW = 19.620, p <.001). When not closely led, females often (24/54, 44%) oriented to hoods, whereas closely led females rarely did (4/52, 8%). In two of the latter four cases, and in eight cases total, males also approached the hood models, not their burrow openings. Crabs that stopped at the models often probed the sand where the burrow opening should have been. Both sexes sometimes visually orient to hoods, and they apparently recognize them as cues to the presence and location of burrows.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The purpose of this study was to determine whether and how a female response to the sand hoods built by courting male U. musica selects for hood building by increasing the mating frequency of hood builders. We recorded the responses of wandering females to courting males, but we do not know if all females were receptive. This probably has not biased our results because both receptive and unreceptive females differentially approached hood builders at the same relative rates.
Receptive females significantly more often approached courting hood
builders than nonbuilders, and builders significantly more often attracted
both receptive and nonreceptive females than did nonbuilders. Once attracted
to males' burrows, receptive females were equally likely to stay and mate
whether the male had a hood or not. Female U. beebei who enter males'
burrows also show no preference for pillar builders
(Christy, 1988b). Hoods and
pillars may attract females, but they apparently do not subsequently affect
mate choice.
Pillar building by U. beebei is a condition-dependent behavior
(Backwell et al., 1995) and
pillar builders allocate more time, and presumably more energy, to waving at
the expense of feeding compared to nonbuilders
(Christy, 1988b). We also
found this pattern when we compared the behavior of hood-building and
nonbuilding U. musica. The presence of a hood, a male's bright white
body color, his energetic claw waving without feeding, and perhaps other
correlated display traits all possibly contribute to his attractiveness.
We did hood removal and addition experiments to control for the possible effects of the behavioral and color differences between builders and nonbuilders on their attractiveness. We first showed that hood removal did not change male courtship behavior, and we assume the same for hood addition. Hood builders without their hoods were significantly less attractive than were builders with their hoods, but they were significantly more attractive than were nonbuilders without hoods. Hence, hoods made males more attractive, but when they were removed, other traits of hood builders contributed to their greater attractiveness. When we added hood models to nonbuilders' burrows, we increased their attractiveness to that of hood builders with natural or model hoods, again showing that hoods make males attractive. However, in this experiment, the differences in behavior and color between builders and nonbuilders, both with hoods, did not measurably affect their attractiveness; the contribution of hoods to attractiveness was paramount. Finally, the displaced hood experiment demonstrated unequivocally that females approach hoods, especially (40% of approaches) when males do not closely lead females to their burrows. These three experiments provide strong evidence that hood builders are preferentially attractive because courted females differentially orient to and approach hoods when they leave a male's burrow and are not closely led to the next one by another male. Why are hoods attractive in this specific spatial, temporal, and social context?
Fiddler crabs use vision to locate their burrow openings only at very close
range (Zeil, 1998;
Zeil and Layne, 2002).
Resident crabs that are feeding away from their burrows
(Cannicci et al., 1999;
Zeil, 1998) and crabs that are
moving between burrows (Zeil and Layne,
2002) use a nonvisual mechanism, probably based on leg odometry
(Zeil and Layne, 2002), to
integrate their movements away from their burrows so that they can return
quickly and directly to them. This mechanism is manifest by the frequent small
changes a crab makes in its body orientation that keep its transverse axis
nearly aligned with the bearing to its burrow
(Zeil, 1998;
Zeil and Layne, 2002). Female
U. musica used this mechanism as they departed from males' burrows.
However, as they moved farther away, we often noted that they abruptly changed
their body orientation and apparently abandoned their path map to the burrow.
This was most obvious when they made clear angular changes from their
departing directions and either followed males to their burrows or approached
males who waved at them but stayed close to their burrows. This is the precise
spatial and temporal context in which hoods attract females, perhaps because
they are a conspicuous and reliable visual guidepost to males' burrows. Thus,
hoods may elicit landmark orientation, visually mediated differential
orientation, vertical objects (Langdon and
Herrnkind, 1985). This behavior is expressed soon after crabs
settle from the plankton (Herrnkind,
1972), is thought to reduce predation risk
(Herrnkind, 1983), and is
widespread in the genus (Christy,
1995).
Bird bowers usually are built in dense vegetation where only nearby females
can see them (Andersson, 1991;
Borgia, 1995). In contrast,
crabs and cichlid fishes build their structures in relatively open habitats
where distant females may see and be attracted to them, increasing the rate
that builders encounter and court females. Thus, crab and fish courtship
structures might function like the long-range advertisement calls of many
passerines, anurans, and orthopterans. Courting male U. musica, and
especially U. beebei (Christy,
1988b), often occur in high-density patches. Courting males of
other fiddler crabs also aggregate, forming groups some have compared to leks
(Croll and McClintock, 2000;
Greenspan, 1980). U.
beebei and U. musica females may differentially orient to
aggregations of courting males (Zucker,
1981; but see Christy,
1988a), but the signals or cues that may attract them are
unknown.
We studied the possible mid-range (roughly 1 m) attractiveness of
hoods by asking whether they affect the rate that males, within the
high-density areas where we observed them, encounter and court females.
Visitation rates to hood builders with their hoods intact and removed fit the
rates expected from their differential availability for visits and their
differential attractiveness. Hence, distant females probably do not orient to
hoods. The hood addition experiments gave an unexpected result. Nonbuilders
with models received more visits than did nonbuilders without models. However,
when we corrected for differences in the availability of males for visits and
in their attractiveness to females per courtship, nonbuilders without model
hoods received about 30% more visits than expected. This suggests that there
may be a cost to having a hood that sometimes exceeds the benefit due to the
attractiveness of this structure. One possibility is that a hood may block a
sector of a male's vision (Zucker,
1974), preventing him from seeing and courting females who pass
behind his hood. However, we cannot explain why we may have detected this cost
in only one series of observations.
We have identified a female response to hoods that establishes a consistent
relationship between hood building and male courtship success and thus selects
for this behavior. Our results do not exclude the possibility that hood
building is sexually selected by other mechanisms. During the displaced hood
experiment, in 8 of 213 courtships, males oriented to the hood models, not to
the openings of their burrows. Nearly every day during this study we saw a few
bright-white males follow females as they responded to courtship from other
males. These rogue males did not have burrows. They courted and threatened the
females they followed, and they fought the males at the burrows they visited.
We twice saw resident males become rogues. Both were nonbuilders that had
followed females to neighbors' burrows and then were unable to relocate their
own burrows, despite searching for them in the generally correct area
(Zeil, 1998). These
observations suggest that a male's path integration mechanism sometimes fails
or becomes unreliable. When it does, he may use his hood as a guidepost to
relocate his burrow. Thus, hood building may be sexually selected both because
females are preferentially attracted to hoods and because hoods increase male
resource-holding ability.
The possibility that hoods currently have two sexually selected functions
suggests a new avenue for understanding how structure building may have
evolved. Initially, structures must have been too small to be conspicuous to
relatively distant females, but they may have made burrow openings more
visible to males as they searched for them close by. Even now, some species of
fiddler crabs make low lips or rims
(Christy et al., 2001) that
perhaps only help males find their burrows. In some species, directional
selection favoring larger structures for males might have made them large
enough to elicit landmark orientation from mate-searching females. Thus the
function of hoods as a sexual signal that we have demonstrated in this study
may have arisen as an incidental effect of the function of proto-hoods for
male orientation, with both functions now capitalizing on landmark
orientation, a behavior that is selected by predation.
|
ACKNOWLEDGEMENTS |
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We thank W. Eberhard, M. Jennions, and J. Zeil for their detailed and helpful critical comments on an earlier draft of this paper and the Smithsonian Tropical Research Institute and the Japanese Ministry of Education, Culture, and Science for their generous support.
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