JOURNAL OF CRUSTACEAN BIOLOGY, 28(2): 328–333, 2008
IS THE HATCHING CLOCK OF FIDDLER CRAB LARVAE (UCA THAYERI)
PHENOTYPICALLY PLASTIC?
Catherine E. Christopher, Michael Salmon, and Richard B. Forward, Jr.
(CEC, MS) Department of Biological Sciences, Florida Atlantic University, 777 Glades Road,
Box 3091, Boca Raton, Florida 33431, U.S.A.
(CEC: [email protected]) (MS, correspondence: [email protected]);
(RBF) Nicholas School of the Environment and Earth Sciences, Duke University Marine Laboratory,
135 Duke Marine Lab Road, Beaufort, North Carolina 28516, U.S.A.
(RBF: [email protected])
ABSTRACT
Larval release by adult fiddler crabs occurs during the ebbing tides, but its timing relative to the day-night and tidal amplitude cycles
depends upon tidal form, e.g., shows phenotypical plasticity. Crabs (Uca thayeri) from Florida’s East Coast are exposed to semidiurnal
tides and release their larvae at night, whereas crabs from Florida’s West Coast are exposed to mixed tides and release their larvae during
the afternoon. The purpose of this study was to determine whether the larvae would hatch at other times, specifically those dictated
by females from a different coast. To find out, clusters of eggs at similar stages of development, 24-72 h in advance of release, were
reciprocally transferred between females from each location. Release of both the transferred and maternal larvae occurred synchronously,
at the time dictated by the female’s tidal regime. These results indicate that fiddler crab embryos can either advance or delay their hatching
clock to match the temporal regime dictated by a brooding female.
KEY WORDS: hatching, rhythms, Uca, phenotypic plasticity, fiddler crabs
change, but in an estuary with semi-diurnal tides, their
rhythm is tidally synchronized. Exposing non-tidal crabs to
tidal changes in salinity entrains their hatching rhythm to the
tides, whereas maintaining tidal crabs under non-tidal
conditions while exposing them to a day-night cycle induces
a diel hatching rhythm (Forward et al., 1986; Forward et al.,
1982). Female sand fiddler crabs (Uca pugilator) transferred
reciprocally between sites exposed to diurnal and mixed
tides will, within weeks, release their larvae at times appropriate to the new tide (Morgan 1996b). Another species
(U. thayeri), exposed to mixed tides on Florida’s West
Coast, releases its larvae during the afternoon (Kellmeyer
and Salmon, 2001), but within 4 weeks after crabs are
transferred to Florida’s East Coast they release their larvae
at night in synchrony with the local population (Weaver and
Salmon, 2002).
Adult fiddler crabs, then, can change their reproductive
rhythms to match local conditions. Their larvae, however,
have less time to adjust since embryological development is
completed within two weeks (DeCoursey, 1979). In addition, larval nervous and sensory systems may be incapable
of normal function until shortly before hatching. Since
during development the eggs are sequestered between the
female’s pleon and thorax, the embryos may also be sheltered from exposure to the appropriate zeitgeber. Yet immediately after release, the larvae must respond by vertical
migration to local tidal cues (Forward and Tankersley,
2001). The timing of those cues varies with tidal form.
The purpose of this study was to determine whether
fiddler crab embryos have the capacity to hatch at times
other than those anticipated by their hatching ‘‘clock’’.
Fiddler crabs are interesting subjects for these experiments
because both females and their clutches have a clock that
INTRODUCTION
Most organisms express different phenotypes, (physiology,
morphology, or behavior) in different environments
(Trussell and Smith, 2000; Agrawal, 2001; Pigliucci,
2005). These responses are hypothesized to promote survival and reproductive success over the range of conditions
that individuals are likely to encounter both in space, and
over time (Price et al., 2003).
Tidal rhythms of crustacean behavior (activity, feeding,
migration, and reproduction) vary among species exposed
to different tidal patterns (tidal ‘‘forms’’; Barnwell, 1976;
Palmer, 1995). Populations within species exposed to different tidal forms may show temporally distinct reproductive
rhythms (Barnwell, 1968; Forward, 1987; Morgan, 1996a)
because tidal currents are important for larval transport and
dispersal. Currents that occur during some phases of lightdark cycle, or that vary in strength, are more favorable for
dispersal than others (Morgan, 1995).
Differences in rhythms among populations might depend
upon either of two mechanisms. One hypothesis is that
individuals residing in any one area differ genetically from
those in other geographic areas and are uniquely adapted to
the particular tide expressed locally. The second hypothesis
is that all individuals among the populations retain the
flexibility to respond adaptively to any tidal form they
encounter, i.e., they are phenotypically plastic.
One way to distinguish between these alternatives is to
transfer individuals among habitats with different tides.
Experiments of this nature have demonstrated that adult
brachyuran crabs are phenotypically plastic. For example,
larval release of Rithopanopeus harrisii occurs on a diel
cycle in upper estuarine locations not exposed to tidal
328
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CHRISTOPHER ET AL.: LARVAL PHENOTYPIC PLASTICITY
dictates when hatching should occur. Experimental studies
(De Vries and Forward, 1991a, b) indicate that peptide
pheromones control both hatching synchrony and the timing
of larval release. However, in those studies both the female
and her larvae had clocks that were in phase. In this study,
we established experimental groups of crabs that brooded
embryos whose clocks differed in phase from those of the
female. Through this technique, we could determine if the
larvae were phenotypically plastic with respect to hatching
time.
We used Saigusa’s (1993) technique to exchange egg
clusters, at similar stages of development, between ovigerous females (U. thayeri) captured on opposite coastlines
of Florida. After the exchange, females brooded a clutch
containing both their own and a donor’s eggs. We hypothesized that if the larvae of each population had a genetically
fixed rhythm, hatching and release might occur twice: at
a time dictated by both the exchanged larvae and the
female’s own clutch. However, if the larval rhythm was
phenotypically plastic, the entire clutch should be released
only once, and at a time dictated by the female. Our results
provide support for the hypothesis that the larvae show
phenotypic plasticity.
MATERIALS AND METHODS
Collection Sites
The east coast site (Mangrove Park in Boynton Beach, Florida, U.S.A.;
26.54 83 N lat., 80.05 33 W long) was a 13.9 km2 area drained by several
tidal creeks that flowed east into the intracoastal waterway. Tides at this site
were semi-diurnal. Ocean water entered the waterway from the Boynton
Inlet, located 2.2 km to the north. Vegetation inside the park had grown
naturally since 1940, and was dominated by red (Rhixophora mangle),
white (Laguncularia racemosa), and black (Avicennia germinans) mangroves. The west coast site (Rookery Bay National Research Reserve) was
located just south of Naples, Florida (26.02 41.8 N lat., 81.42 30.0 W
long.). Tides at this site were mixed. Mangrove stands were drained by
several small (1-2 m wide) tidal streams that flowed west into the Gulf of
Mexico. Mangroves species composition was similar to the east coast site.
Crab Maintenance
Ovigerous females were captured at low tide from their ‘‘chimney’’ or
‘‘funnel’’ burrows (Salmon, 1987). Collections from each site were made
every 2-4 weeks between May-October, 2003-4, generally 7-10 d prior to
an anticipated peak in the time of larval release at each site. Although
everywhere abundant, crabs were most easily captured at the tidal creek
banks where there were fewer mangrove roots.
Crabs were transported within three hours to a windowless laboratory
at Florida Atlantic University (Boca Raton, Florida, U.S.A.) where they
were maintained on a 14L:10D photocycle (controlled by a timer) and
temperature of 26 6 28C. Crabs from each population were marked on the
carapace with waterproof ink to facilitate identification by collection site
and date. Marked crabs were placed in glass aquaria (50.8 3 25.4 3 30.5 cm
tall) containing a shallow pool of filtered seawater and several bricks with
holes that served as individual shelters. Crabs were fed TetraminÒ flake
food and given new seawater (salinity of 35 ppt) each day.
Fiddler crabs incubate eggs for 12-14 d at summer temperatures
(DeCoursey 1979; Christy 1982). During embryological development the
color of the sponge egg mass gradually changes from the yolk’s color (red/
purple) to blackish-grey (the color of the embryos’ compound eyes and
melanophores), as most of the yolk is consumed. Eggs that will hatch within
24 h contain almost no yolk. The ovigerous crabs that we collected had eggs
in different stages of development. Some hatched immediately (the evening
of the day the crabs were collected) while others hatched within a week
after the females were captured.
Sponges that were in an advanced stage of development (hatching
anticipated within 3-6 d) were staged by inspecting 2-3 eggs from each
female at 100 3 magnification. Any female whose embryos would hatch
within 24-72 h was transferred to a vertically-suspended incubation tube
(20.0 cm long 3 15 mm inside diameter) made of opaque plexiglasÒ. The
tube simulated a breeding burrow, the site of larval release. A rod through
each end of the tube prevented the crab’s escape. The bottom of each tube
was submersed to a depth of ;2 cm within a small glass jar (6.0 cm
diameter, 8.0 cm high), filled with seawater that was changed daily. Enough
water was present in each tube to enable females to release their larvae into
the jar, which served as a reservoir.
Females in incubation tubes were maintained at temperatures and on
a photocycle identical to females in the aquaria, but were not fed. The tubes
contained two groups of crabs: those from each coast with their own
clutches (controls), and those from each coast with sponges consisting of
their own eggs and the eggs of a female from the opposite coast
(experimentals).
Egg Cluster Exchange Between Females
Reciprocal exchange of egg clusters was done during the day, 24-72 h
before an anticipated release, using methods developed by Saigusa (1993).
Pairs of females (one crab from each coast) were selected for surgery if their
eggs were at similar stages of development.
Both crabs were temporarily immobilized by a 5-7 min exposure to cold
inside a refrigerator. The pleon of each cooled female was held away from
the thorax to expose the sponge. A fine scissors was used to cut the last two
of the eight pleonal setae at their base. The two setae stalks were then tied
together in the center of a length of fine thread.
Egg transfer was completed after each crab was again briefly exposed to
cold. The pleon was held away from the thorax so that the egg clusters from
the donor female could be positioned where the egg clusters had been
removed from the recipient female. The thread was wrapped twice around
the pleon to hold the clusters in position, and the thread ends tied together
outside the pleon so that its movement was not impeded. After surgery,
each female was placed in an incubation tube. Chelae were not removed
from the crabs since (with one exception) surgically altered females did not
dislodge or consume any of their eggs.
Timing of Larval Release
Larval release by fiddler crabs held under a natural photocycle in the
laboratory occurs on the same day as larval release by females at the
collection site (DeCoursey, 1979, 1983; Bergin, 1981; Christy, 1982;
Forward et al., 1986; Salmon et al., 1986). However, under laboratory
conditions, the timing of release relative to high tide can be more variable
(Kellmeyer and Salmon, 2001; Weaver and Salmon, 2002). In the field,
release by other species of fiddler crabs is highly synchronized with the
tides and occurs either at slack high tide, or within minutes after the tide
begins to ebb (Salmon et al., 1986).
We inspected the jars under each incubation tube at 30 min intervals,
beginning one hour before the afternoon high tide (at Naples) and ending
three hours after the evening high tide (at the Mangrove Park). After the
lights in the laboratory were switched off, inspections were made using
a small flashlight dimmed with a red filter. If larvae were found, the female
was removed from her incubation tube to determine if all of her larvae had
been released.
Spent East Coast crabs were released the next day at the Mangrove Park
site; those from the West Coast were returned to their capture site 1-2 weeks
later, when new ovigerous crabs were collected. Released larvae were
transferred to a large seawater-filled bucket whose contents were emptied
during the next nocturnal ebbing tide into a tidal creek at the Mangrove
Park.
Data Analysis and Statistics
All crabs released their larvae within ;3 min. Larval release time was
placed within its 30 min inspection interval and was converted to an angle,
relative to the onset of darkness (08; defined as sunset on that date, þ30
min). If a release occurred after the onset of darkness, time was converted
into an angle that increased by 158/h; if a release occurred before the onset
of darkness, the angle decreased (from 3608) by 158/h. For example, if
a female released her larvae 3 h after dark, her release angle was 458; if she
released larvae 3.5 h before dark, the release angle was 3178 (3608-538).
A similar procedure was used to record release time relative to the onset
of high tide (08). Release times relative to high tide were plotted to the
nearest h (6 298).
Angles relative to darkness for the control or experimental females from
each coast were grouped, then analyzed using circular statistics (Zar, 1999)
to determine a group mean angle and r-vector (measure of dispersion,
varying between 0 [randomly scattered angles] to 1.0 [all angles identical]).
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 28, NO. 2, 2008
Fig. 1. East coast Uca thayeri. Circle diagrams show the distribution of
larval release times for the control (left column) and for the experimental
(right column) crabs. A, B, release times relative to the onset of darkness
(08); C, D, release times relative to high (08) and low (1808) tide. Control
crabs (n ¼ 30) carry their own eggs; experimental crabs (n ¼ 17) bear their
own eggs, plus those transferred from females captured on the West coast
of Florida. Large triangle is the approximate time of sunrise. Small triangles
indicate when each female released her larvae. Symbols: a, group mean
angle (also shown by the black arrow outside each plot); r, dispersion;
p, Rayleigh probability.
Rayleigh tests were used to determine whether each distribution was
composed of a uniform distribution of angles. That hypothesis was rejected
when Rayleigh probabilities were 0.05.
Watson two-sample tests (Zar, 1999) were used to compare distributions
of release relative to the light-dark cycle between (i) crabs from each coast
that were brooding their own eggs, (ii) experimental crabs from each coast
brooding both their own and transferred eggs, and (iii) control and
experimental crabs from the same coast. The null hypothesis of no
difference between these groups was rejected when Watson U2 probabilities
0.05.
RESULTS
Larval Release by the Control Crabs
Control crabs from Boynton Beach most often released their
larvae between dusk and midnight (Fig. 1A), on average one
h (158) after the onset of darkness. Control crabs from
Naples (Fig. 2A) released their larvae during the day, on
average about 7 h before dark. Both groups released their
larvae primarily near high tide (Figs. 1C, 2C), but this
timing was more variable among the West than among the
East coast crabs.
Both the dark-light and tidal distributions of the control
crabs were significantly clustered (Rayleigh P , 0.001).
Larval release by the West coast crabs was significantly
Fig. 2. West coast Uca thayeri. Circle diagrams show the distribution of
larval release times for the control (left column) and for the experimental
(right column) crabs. Control females (n ¼ 27) carry their own eggs;
experimental females (n ¼ 16; one female ate her brood) bear their own
eggs, plus those transferred from females captured on the East coast of
Florida. Format and symbols are as in Fig. 1.
earlier in the day than larval release by the East coast crabs
(Watson U2 ¼ 1.043, P , 0.001).
Larval Release by the Experimental Crabs
All of the experimental crabs with transferred embryos
released their larvae at one interval; there were no cases of
multiple releases at different times of the light:dark cycle.
Experimental crabs from Boynton Beach released their
larvae during the dark period, on average about 3.5 h after
the onset of darkness (Fig. 1B). Experimental crabs from
Naples crabs released their larvae during the day (Fig. 2B),
again averaging ;7 h before darkness onset. Both experimental groups released their larvae primarily near high tide
(Figs. 1D, 2D).
Both the dark-light and tidal distributions of the
experimental crabs were significantly clustered (Rayleigh
P , 0.001). The timing of larval release relative to the lightdark cycle differed significantly between the two experimental groups (Watson U2 ¼ 0.730, P , 0.001).
Larval Release by Crabs from the Same Coast
Both the control and experimental crabs from Boynton
Beach released their larvae primarily in the evening (Fig.
1A, B) and at high tide (Fig. 1C, D). However, the majority
of the control crabs released during the high tides that
occurred near dusk whereas all of the experimental crabs
CHRISTOPHER ET AL.: LARVAL PHENOTYPIC PLASTICITY
released larvae during high tides that occurred at 2-3 h later.
The control and experimental groups differed significantly
in timing (Fig. 1; n ¼ 47, Watson U2 ¼ 0.224, P , 0.05).
The control and experimental crabs from Naples showed
no statistical differences in timing of larval release relative
to the light-dark cycle (Fig. 2A vs. 2B; n ¼ 43, Watson U2 ¼
0.151, P , 0.10). However, timing relative to the tidal cycle
(Fig. 2C vs. 2D) differed significantly between the groups
(Watson U2 ¼ 0.339, P , 0.001).
DISCUSSION
Uca thayeri from the east and west coast of Florida are
exposed to different forms of the tides, and differ in larval
release timing (Kellmeyer and Salmon, 2001; Weaver and
Salmon, 2002). On the East Coast, larval release occurs near
high tide during the evening (between dusk and midnight;
Fig. 1) whereas on the West Coast it occurs during the day
in mid-summer (Fig. 2). Our data again confirm those
differences in timing between the populations.
Experimental females received clusters of eggs from
females captured on the opposite coast, enabling us to
determine whether the timing of larval release could be
changed by signals from the larvae. There was no indication
that they could.
The East coast control and experimental crabs showed
statistical differences in release timing relative to the lightdark cycle, but both groups released larvae primarily at
night, and during times shown by crabs in previous studies
that were brooding their own clutches (Kellmeyer and
Salmon, 2001; Weaver and Salmon, 2002). West coast
control and experimental crabs showed no statistical differences in release timing relative to the light-dark cycle
(Fig. 2A, B).
Control and experimental crabs from the East coast
showed no statistical differences in release timing relative to
the tides (Fig. 1C, D), but control and experimental crabs
from the West coast did (Fig. 2C, D). Those differences
occurred because release timing relative to the tides was
more variable among the control than among the experimental crabs. However, if the transferred larvae had
influenced release timing the experimental crabs should
have shown greater variability than the controls.
Finally, all females, regardless of location, released their
larvae once rather than in two episodes (as hypothesized if
the clocks of larvae from each coast could induce pleonal
pumping in the experimental females). Taken together, these
results are consistent with the hypothesis that females and
not their larvae determine the exact time of larval release
(DeVries and Forward, 1991a).
Adaptive Significance of Phenotypic Plasticity
Since the larvae of fiddler crabs may invade coastlines
exposed to different tidal forms, it has been proposed that
adult crabs must adapt to any tidal form (Morgan, 1996b;
Thurman, 2004). Evidence that the adults possess this
capacity comes from translocation experiments. These have
shown that mature females can alter the time of larval
release within a few weeks after they are exposed to a new
tidal regime (Morgan, 1996b; Weaver and Salmon, 2002).
Such a capacity is also adaptive because most fiddler crab
331
species are widely distributed along coastlines that are
exposed to different forms of the tide.
Uca thayeri is typical of many fiddler species. It is found
in subtropical Florida, throughout the Caribbean, and south
to Brazil. Across this space, it is exposed to at least three
tidal forms. Twelve additional fiddler crab species are found
on coastlines inundated by all tidal forms (Crane, 1975). Of
the 97 described species of Uca, 61 (63 %) are distributed in
areas inundated by at least two tidal forms. The largest
assemblage of fiddler crab species is found on the Caribbean
and Pacific coast of Central America where they are exposed
to either a mixed or a semi-diurnal tide (Crane, 1975).
Phenotypic plasticity among the larvae of semi-terrestrial
crabs should be favored by natural selection for the same
reason that it is favored among the adults: because the larvae
must be capable of temporally appropriate responses under
any tidal regime they encounter. That plasticity consists of
two sets of responses: those governing the timing of larval
behavior after release, and those governing the timing of
embryo behavior before release.
After release, the larvae vertically migrate, a response that
promotes their transport and dispersal away from adult
release sites (Forward and Tankersley, 2001). How the
embryos obtain this information in advance of release is
unknown. In one crab species (Carcinus maenas), even
larvae brooded by females maintained for months under
non-tidal conditions (but a 24 h light-dark cycle) in the
laboratory show vertical migration rhythms appropriate to
the tides at the collection site. These results led to the hypothesis that the larvae inherit a tidal rhythm that is triggered
by the release act itself (Zeng and Naylor, 1996). However,
in fiddler crabs the embryos apparently also respond to local
cues that can release different rhythms of vertical migration.
Recent studies (Lopez-Duarte and Tankersley, in press)
demonstrate that newly released fiddler crab zoeae, over their
first 96 h of swimming, show endogenous rhythms of vertical migration specific to the tidal form at the release site.
Periodicities among populations are expressed as 12.4 h
under a semidiurnal tide, 24.8 h under a diurnal tide, and
either 12.4 or 24.8 h under a mixed tide pattern.
In contrast to the rhythmic behavior of larvae during
vertical migration, larval release in most crabs is a single
event; in fiddler crabs it is completed within minutes
(DeCoursey, 1979), suggesting that selection for tight
synchrony should dominate both adult, and larval, behavior.
For adult semiterrestrial crabs, the likely reason is that
females while releasing larvae are more vulnerable to
predators (DeCoursey, 1979; Forward and Lohmann, 1983).
They either leave burrows to migrate to suitable release sites
(rivers, tidal creeks or the ocean among supratidal species;
Saigusa, 2000), or open their burrows under water (intertidal
species like fiddlers) to release their propagules into the
water. Doing so generates mechanical (currents produced by
pleonal pumping) and chemical (odor trails from the larvae)
cues that could reveal the female’s location to a potential
predator.
The mechanisms underlying hatching and release among
crabs have been studied in only a few species, but
nevertheless a pattern has emerged. In subtidal species,
control of hatching and release resides in the brood. For
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 28, NO. 2, 2008
example in the blue crab (Callinectes sapidus), the larvae
hatch synchronously without any signal from the female.
Hatching is initiated both by osmotic swelling of the eggs
and by enzymes secreted by the larvae some time in advance
of release, that break the outer egg membrane and allow the
zoeae to hatch. At the time of larval release, the embryos
release a pheromone which results in the synchronous
release of larvae by the female (Tankersley et al., 2002). A
similar mechanism of control is hypothesized to occur in the
xanthid crab R. harrisii (Forward and Lohmann, 1983), and
was demonstrated to occur in the grapsid crab, Neopanope
sayi (De Vries and Forward, 1989, 1991b). In N. sayi, eggs
detached from females a few hours before hatching, and
either kept in still seawater or in seawater that was periodically agitated (to mimic pleonal pumping by the female
during release), hatched in synchrony with eggs left on the
female. Furthermore, these larvae under all conditions were
viable and capable of swimming (De Vries and Forward,
1991a).
Among an intertidal (U. pugilator) and supratidal (Sesarma cinereum) species, enzyme release by developed
embryos inside the eggs is triggered in some unknown
way by a signal from the female (De Vries and Forward,
1991b). When eggs are detached from females, this signal is
absent. Hatching still occurs (indicating that the larvae
possess a hatching ‘‘clock’’), but is delayed by several hours
compared to the hatching time of larvae still attached to the
female. Some of the larvae that hatch from detached eggs are
incapable of swimming (17% in U. pugilator; 50% in
S. cinereum), and have reduced viability (De Vries and
Forward, 1991a).
These results show that in intertidal and supratidal crabs,
females control both the onset of hatching and larval release
so that both occur in close temporal association. By
coupling the two processes closely in time, the brood may
avoid any danger of dessication between the time of
hatching, and the time it takes the female to migrate to the
release site. That danger is most likely among the supratidal
than among the intertidal species, which may explain why
the effects of egg detachment on hatching time and larval
survival are more extreme in S. cinereum than in U.
pugilator (De Vries and Forward, 1991b).
The tightest control by a female crab occurs in S.
heamatocheir, a graspid living in forests. Females migrate
over land at night to freshwater rivers to release their larvae,
which are swept down current to the sea where development
is completed. In this species, eggs detached from the female
more than 50 h prior to the time of release failed to hatch,
whereas those detached from the female within 49 h hatch,
although somewhat later and with less synchrony than eggs
left on the female (Saigusa, 1992).
Thus, control of hatching and release shifts from the
embryos in subtidal species, to the female among intertidal
and supratidal species, probably because the embryos in the
latter group cannot determine when females will locate
suitable release sites (De Vries and Forward, 1991a).
Evidence in support of this hypothesis comes not only from
the experiments cited above, but also from the positive
correlation between the degree of control exerted by
females, and the degree of terrestriality shown by the
adults. As a consequence the larvae of semiterrestrial crabs
after hatching are programmed to cling to their empty egg
membranes until they receive a release signal from the
female. That response probably explains why eggs, transferred to females of U. thayeri with different timing
programs, hatch synchronously with the female’s brood,
and why the larvae are phenotypically plastic. They must
‘‘wait’’ for the female to tell them that a release site (water)
has been found.
ACKNOWLEDGEMENTS
This study was completed by CEC as a Masters thesis. We thank A. Marsh
and D. Gawlik for serving on the thesis committee; their suggestions, and
those of R. Tankersley and an anonymous referee, improved the manuscript. J. H. Cohen provided statistical advice. The staff of the Rookery
Bay National Research Reserve allowed us to collect crabs on the West
Coast. C. Whelan, A. Broner, N. Desjardin, E. King, and K. Pancake
assisted in the field work. Financial support was provided by the Nelligan
Fund, Florida Atlantic University.
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RECEIVED: 9 June 2007.
ACCEPTED: 19 September 2007.