A M . ZOOLOCIST, 8:569-583 (1968).
The Role of Rhythmic Systems in the Adaptation of Fiddler Crabs to the
Intertidal Zone
FRANKLIN H. BARNWELL
W. C. Allee Laboratory of Animal Behavior, University of Chicago,
Chicago, Illinois 60637
SYNOPSIS. Fiddler crabs inhabiting the intertidal zone must adapt their activity to
both the day-night cycle and the cycle of the tides. The tidal cycle imposes on the
animals a rhythmic alternation between terrestrial and marine periods of existence. At
the same time the crabs are influenced by the day-night cycle, since they exhibit
specific diurnal and nocturnal habits. Moreover, the interaction of daily and tidal
rhythms may give rise to semi-monthly variations in activity.
It is now well established that persistent daily and tidal rhythms in physiological
processes underlie rhythmic variations in the behavior of crabs in the field. The present
paper reviews more recent studies, which have compared the persistent rhythms in
crabs from different tidal and non-tidal regions. Rhythmic patterns recorded in
the laboratory are found to be closely correlated with tidal conditions in the native
habitat of the crabs. It has also been shown that the persistent pattern can be
modified by transplanting crabs to the intertidal zone of another coast where they are
exposed to tidal cycles which differ in form from those in the original habitat.
Fiddler crabs inhabiting the intertidal
zone are exposed to both the 24-hour daynight cycle and the cycle of the tides. The
tides vary in their pattern from region to
region, but in their period they tend to
average either 12.4 or 24.8 hours.
How the fiddler crabs adjust their activities to these two major environmental
cycles of only slightly different periods is
an intriguing problem in biological timing. Our present understanding of the
nature of this adjustment has been advanced by two separate lines of investigation. On the one hand, the field approach
has provided descriptions of daily and
tidal rhythms in the behavior of fiddler
crabs in their natural habitat. On the other hand, laboratory studies have demonstrated that various physiological processes
in fiddler crabs may exhibit daily and
tidal rhythms that persist even in constant
light and temperature. These persistent
rhythms have been shown to be under the
This work was supported by funds allocated to
1'rof. Frank A. Brown by the Office of Naval
Research (Contract 1228-30) and the National
Science Foundation (Grant GB 3481).
I thank Mr. J. Y. Christmas for his generous
assistance on my visits to the Gulf Coast Research
Laboratory.
control of specific mechanisms, the socalled "biological clocks".
This paper considers certain ecological
aspects of "clock-timed" rhythms in
fiddler crabs. First the results of field
studies are reviewed. Then an account is
given of persistent rhythms in crabs from
different tidal and non-tidal habitats. Finally an experiment is described in which
a persistent semi-diurnal tidal rhythm of
locomotor activity is induced in fiddler
crabs from a region of diurnal tides.
RHYTHMIC BEHAVIOR UNDER NATURAL CONDITIONS
The general pattern of activity of intertidal fiddler crabs is well known. As their
habitat is exposed by the ebbing tide, the
fiddler crabs emerge from their burrows
onto the surface. Morphological, physiological, and behavioral adaptations fit the
crabs for brief periods of active terrestrial
existence. Observations of a colony of
fiddler crabs at low tide may reveal die
crabs engaged in feeding, repair of burrows, and ritualized courtship and combat. With the return of the tide the crabs
withdraw into their burrows. The animals
may appear to anticipate the tide by en-
569
FRANKLIN H. BARN WELL
APR
I -
MAY
I
0600
0900
1200
TIME OF DAY
1500
1800
RHYTHMIC SYSTEMS IN FJDDLER CRABS
FIG. 1. Number of males displaying during low
tides in a captive colony of U. maracoani in Trinidad. Thick bar, more than half of the males
displaying: thin bar, less than half displaying; cir-
tering and plugging their burrows before
the water reaches them (Altevogt, 1957),
or they may linger on the surface and
continue to feed (Teal, 1959) and even
to display1 under several inches or more
of water. Flooding of the intertidal zone
represents for the crab a period of confinement within its submerged burrow until the tide has turned and the region is
again exposed to the air. Thus, each tidal
cycle imposes upon the crab a regular
alternation between terrestrial and marine phases of existence. From consideration of this pattern it is obvious that
tidal rhythmicity is an essential feature of
the terrestriality of intertidal fiddler
crabs.
571
tie, no displays; enclosed circle, no observations,
Bar or circle is centered on the time of low tide,
Five days of heavy rainfall are indicated. Data from
Crane (1958).
level of its display by 0830 and had practically ceased waving by 1000. The more
advanced U. annulipes did not display
fully until about 1000 and thereafter continued to wave into the late afternoon.
In contrast to the diurnal behavior recorded for tropical forms, a temperate species, U. pugilator, was observed many
years ago to be active during both diurnal
and nocturnal low tides (Verrill and
Smith, 1873). Field studies in recent times
have demonstrated that this species, as
well as others in temperate regions, not
only displays during daytime low tides
but also carries on courtship behavior at
night by means of acoustical signals (Altevogt, 1962; von Hagen, 1962; Salmon,
1965, 1967).
The fiddler crabs also exhibit adaptaThe time at which intertidal fiddler
tions to the 24-hr day-night cycle. The
elaborate species-typical waving displays crabs are exposed to day or night condiof the males and the accompanying pig- tions on the surface is determined by the
mentary changes are of functional signifi- time of low tide, which itself shifts syscance only during the daylight hours tematically across the 24 hours of the sowhen they can be perceived by other lar day at an average rate of 50 minutes
crabs. Crane (1958) has observed that per day. In a region of semidiurnal tides,
where there are two low tides a day, this
tropical species of Uca are largely diurnal
and include among their number those means that when low tide has occurred at
forms in which display and color change a particular hour of the day, it will not
have reached their highest development. recur at that hour until 15 days later. The
Furthermore, she has described an appar- consequences of the daily and tidal inent relationship between the phylogenetic teraction for fiddler crabs were clearly
position of a species and the time of day demonstrated by a series of observations
at which it reaches the maximum in its carried out in Trinidad by Crane (1958).
intensity of display. The period of display A colony of U. maracoani was mainof primitive species is often restricted to tained in captivity in an outdoor terrarithe hours immediately after sunrise, while um. Artificial tides reproduced the daytime
that of more advanced forms is displaced low tide at the coastal mudflat where the
to a later time of the morning. As an crabs had been collected. The intensity of
example, she cites two species observed on display in the colony was determined during
the Island of Pemba, East Africa. The each daytime low tide over a period of 90
primitive U. urvillei reached the highest days. The colony exhibited a daily variation in the level of waving, with the highest
1. A small male specimen of U. pugnax was seen intensity coming between 0800 and 1000.
by the writer to continue waving after it was Because of the daily-tidal interaction, howcovered by at least three inches of water. The ever, maximum waving could take place
observation was made at 1600 on July 16, 1966, at only at fortnightly intervals when the time
the Chapoquok marsh near Woods Hole, Mass.
572
FRANKLIN H. BARNWELL
of low tide coincided with the optimal
time of day (Fig. 1). More recent field work
in Trinidad has suggested that the intensity
of ritualized combats may exhibit a comparable semi-monthly variation (Crane,
1967). In view of the semi-monthly variations in male reproductive behavior, it is
of interest that females of U. tangeri
show a semi-monthly cycle in ovarian activity (von Hagen, 1962).
Crane (1958) has pointed out that differences in the form of the daily cycle of
waving between two species will be
reflected as differences in their semimonthly cycles. A specific example is furnished by the two East African species
already mentioned. The waving of U. annulipes in the late morning and afternoon is favored by low tides occurring
several days later in the semi-monthly cycle than those permitting the waving of
U. urvillei in the early morning. Through
the daily-tidal interaction a phase difference of several hours in the time of
maximum daily display is converted into
a phase difference of several days in the
semi-monthly cycle. These daily and semi-monthly phase differences in courtship
take on a special significance when one
considers that they may contribute to the
reproductive isolation of sympatric species.
The semi-monthly cycles just discussed
appear to result from the tidal scanning
of a species-specific daily pattern. There
is, in addition, a second form of semimonthly cycle which is imposed directly
on the crabs by the semi-monthly variation in the range of the tides. This second
kind of semi-monthly cycle is experienced most obviously by all fiddler crabs
that burrow in the intertidal zone above
the level of the highest neap tides. This
upper region of the shore is exposed to
one or more days of drying each fortnight when the neap tides fail to cover it.
Crane (1941) has described how the variation in tidal range affected the activity of
a colony of U. latimanus inhabiting the
upper level of the beach at La Boca,
Panama. The colony was active at semi-
monthly intervals, on those days when it
was submerged by the highest spring
tides, but during the intervening eight
days when the water did not reach the
upper level of the beach the crabs remained underground in their burrows.
Animals which were dug up during this
period were found to be comatose.
It should be recognized that the genus
Uca is by no means restricted to the intertidal zone. Fiddler crabs are to he found
in burrows above the littoral region and
in large colonies along the banks of rivers
and streams flowing into the sea. The
crabs appear to be capable of adjusting
their activity to non-tidal conditions. Altevogt (1959) has reported that the activities of U. tangeri living around a nontidal pool conformed to a daily pattern
while crabs of the same species in the
near-by intertidal zone were performing
some of the same activities on a tidal
schedule.
PERSISTENT RHYTHMS OF COLOR-CHANGE
The experimental analysis of timing
systems in fiddler crabs was taken up by
F. A. Brown and his students at Woods
Hole, Massachusetts, during the late
1940's. Brown (1965) has reviewed this
work, but certain features of the studies
will be restated here' as a background for
describing more recent experiments and
interpretations. The initial studies at
Woods Hole dealt with the persistent daily rhythm of color-change in U. pugnax
and U. pugilator. The work led to the
discovery of temperature-relationships and
aspects of phase-synchronization, which subsequently proved to be fundamental properties of biological timing systems.
Brown, et al. (1953) later reported that
a tidal variation was superimposed on
the daily rhythm of color-change. Because
the chromatophoric pigments remain
concentrated during the night, the tidal
rhythm can be clearly expressed only during the daytime when the pigment disperses. Tide-related variations in the daily
pattern were reproduced at 15-day inter-
573
RHYTHMIC SYSTEMS IN FIDDLER CRABS
Id
0
/
\ /
10
\ /
II
\
12
/
13
14
15
DAYS
16
17
18
19
\
20
FIG. 2. Representative tide-curve for Pensacola,
Florida, taken from U. S. Coast and Geodetic Sur-
vey, Tide Tables, East Coast of North and South
America.
vals in accordance with the semi-monthly
repetition of the tidal cycle. It was pointed out that interaction of the daily
rhythm and the semi-diurnal tidal rhythm
provided a means for timing the longer
semi-monthly cycle. The authors also
compared the tidal rhythms in crabs collected from two regions where the tides
differed by four hours. In the laboratory
the rhythms were found to differ in phase
by four hours, the amount expected if
each rhythm was set to the time of tide in
the original habitat.
An even more precise adjustment of
phase to local tidal conditions was revealed by a series of experiments with
fiddler crabs from Ocean Springs, Mississippi (Fingerman, 1960). When the persistent tidal rhythms of color-change in
crabs living at different levels of the same
beach were compared, crabs from the
upper level were found to darken in advance of crabs from the lower level. It was
proposed that the difference in time of
darkening was related to the fact that
crabs at the upper level were uncovered
by the receding tide and could emerge
from their burrows earlier in each tidal
cycle than crabs at the lower level. This
hypothesis was supported by the finding
that the difference in phase between the
tidal rhythms corresponded to the number of hours elapsing between the appearance of crabs on the surface at the two
levels.
In view of the very accurate adjustment
in phase of the Mississippi crabs, it was
regarded as paradoxical that the period of
the persistent tidal rhythm should be
12.4 hr instead of 24.8 (Fingerman, 1956;
Fingerman, et al., 1958). The semidiurnal tidal period of 12.4 hr was
thought to be ecologically inappropriate
for the region of Ocean Springs, where
the tides are diurnal and the predominant pattern is one high tide and one low
tide every 24.8 hr. However, a reconsideration of these experiments will show
that the discrepancy between the apparent period of the cycle of color-change
and that of the tides was not as great as
originally suggested. First the method
used to determine the phase-relationship
and period of the tidal component should
be noted. These values were estimated
from hourly readings of the degree of dispersion of melanin between 0800 and
1900 on alternate days. It was concluded
that the tidal rhythm in color-change was
semi-diurnal tidal because the form of
the daily pattern was repeated at approximately 14.8-day intervals. Fingerman assumed that repetition of form would occur at 29.5-day intervals if a diurnal tidal
rhythm were present. This latter assumption is incorrect, as shown by the following example.
In Figure 2 a tide-curve for Pensacola,
Florida, is reproduced from an illustration in the tide-tables of the U. S. Coast
and Geodetic Survey. The curve demonstrates the changes in form that a diurnal
tide undergoes during the course of 11
days. The diurnal inequality in the height
of semi-diurnal tides varies with the declination of the moon. When the declination is large, the diurnal inequality in the
northern Gulf of Mexico is so great as to
efface altogether one of the semi-diurnal
tides. The resulting diurnal, or tropical,
tide is exemplified by the patterns on days
10 through 14 in Figure 2. As the moon
crosses the equator the diurnal inequality
in range of the tides is reduced to the
574
FRANKLIN H. BARNWELL
point where the semi-diurnal, or equatorial, tide is expressed, as on day 16. Movement of the moon into the opposite hemisphere is accompanied by an increase
in the range of the second high tide of
the semi-diurnal pattern and the disappearance of the first high tide. The alternation in the range of the two tides is
seen on day 17 when the high tide which
was dominant on day 10 has disappeared
and the second high tide is emerging during the early morning. The new high tide
will increase in range and shift into the
early afternoon, thereby reproducing the
form of the cycle observed some 15 days
earlier. The repetition of form will not be
exact since the tropical-equatorial sequence is imposed on the tides with a
13.6-day cycle instead of a 14.8-day one.
Nevertheless, the finding that the form ot
a portion of the daily cycle is repeated at
more nearly semi-monthly than monthly
intervals provides no clear basis in itself
for distinguishing between semi-diurnal
and diurnal tidal patterns. It would now
seem that the observed rhythm of colorchange is what might be expected if the
crabs were adapted to the diurnal tides of
the Mississippi coast.
Repetition of pattern at approximately
semi-monthly intervals was observed during the summers of 1955 and 1957 in
fiddler crabs from Ocean Springs. However, during the intervening summer an
unexplained deviation from this pattern
was reported (Fingerman, 1957). Instead
of recurring at 14.8-day intervals, the
maxima thought to result from the interaction of daily and tide-related components were 7.4, 7.4, 11.5 and 14.8 days
apart.
in Figure 3. The curves are from a study
in which metabolic patterns in crabs from
two levels of the same beach were compared (Barnwell and Brown, 1963; Barnwell, in preparation). Very large tiderelated changes in rate are obvious (Fig. 3).
The records selected for Figure 3 also
permit a comparison between tide-related
activity occurring at night and during the
day. It can be seen that crabs of both
species inhabiting the upper level of the
beach exhibited greater total activity during the nocturnal tidal peak than during
the diurnal one, while crabs from lower
in the intertidal zone did not show such
an obvious difference. The day-night
component was much more conspicuous,
then, in crabs living higher on the beach
where they were exposed to terrestrial
conditions for a longer portion of each
tidal cycle. A similar finding was reported
by Fingerman, et al. (1958) when they
compared the patterns of color-change
in crabs living above tidal influence with
those of crabs from between the tidemarks.
As evidenced in Figure 3, and confirmed
by statistical analysis, crabs from the upper
beach tended to reach their maximum
metabolic rate in each tidal cycle from 30
min to 2 hr before those from the lower
beach. However, in contrast to the findings
of Fingerman (1960) on the rhythm of
color-change, the present data revealed no
such consistent difference when the times
of minimum metabolic rate were compared.
In fact, some crabs from the lower beach
reached the minimum rate in each tidal
cycle before crabs from the upper beach.
This difference would be expected if the
time of covering by the advancing tide
were of significance to the animals, since
crabs on the lower level are covered bePERSISTENT RHYTHMS IN OXYGEN
fore those at the upper level.
CONSUMPTION
When the fiddler crab is covered by the
By means of a continuous recording res- rising tide, it may have to alter its metapirometer, Brown, et al. (1954) demon- bolic rate for at least two reasons. In the
strated persistent daily and tidal rhythms first place the level of oxygen in the burin the rate of Oo-consumption in U. pug- row may be reduced, even to the point of
nax and U. pugilator. Examples of the being immeasurably low (Teal, 1959;
variation in metabolic rate are presented Teal and Carey, 1967). Secondly, the
575
RHYTHMIC SYSTEMS IN FIDDLER CRABS
250
u.
200
PUGNAX
ISO
\
100
50
i
0
6 JULY 63
B
7 JULY
8 JULY
i
9 JULY
250
.
200
U. BJGILATOR
150
100
5
\/V"'
50
4 AUG 63
5AUG
FIG. 3. Continuous recordings oC O2consumption
of (A) U. pugnax and (B) U. pugilator from
different levels of the Chapoquoit marsh near
Woods Hole, Massachusetts. Solid line, crabs from
6 AUG
V A
7 AUG
lower level; dotted line, crabs from upper level,
Small triangles indicate the predicted times of high
tide at Chapoquoit. Recordings were made in
constant illumination and temperature.
a much more pronounced component of
nocturnal activity than was shown by U.
pugnax. Presumably the pattern of U. pugilator was related to the high level of
nocturnal courtship which the writer has
observed in this species in the marshes at
Woods Hole.
The most graphic demonstrations of
persistent tidal rhythms in the Woods
Hole species were obtained from U. minax. The record of a female specimen is
presented as an example; the phase relationship between the rhythm of locomotor activity and the tides can be described
PERSISTENT RHYTHMS IN LOCOMOTOR ACTIVITY
by comparing the time of onset of activiThe overt rhythms in metabolic rate in ty with the predicted times of high tide
fiddler crabs were found to reflect rhyth- in the natural habitat (Fig. 4). The time
mic variations in locomotor activity (Ben- of onset occurred in advance of the prenet, et al., 1957). In a recent study the dicted time of high tide for the first 10 days
patterns of locomotor activity in the three of recording. Thereafter the onset shiftspecies of Uca in the Woods Hole region ed to a point which varied from 1-3 hr
have been compared (Barnwell, 1966). after the time of high tide. Then on Sept.
Differences in pattern emerged at the spe- 1 the period of the tidal component incies level and within species. For exam- creased abruptly, and by the end of the
ple, the activity of U. pugilator exhibited experiment on Sept. 6 the time of onset
Oo-consumption of U. pugnax and U.
pugilator is reported to be higher in
water than in air (Teal, 1959). Under
these conditions it would appear to be
advantageous to the crab to reduce its
metabolic requirements and thereby to
prolong a limited supply of oxygen.
Thus, it is possible to view the rhythmic
reduction in metabolic rate and its synchronization with the time of tidal covering as an adaptation to periods of low
oxygen.
576
FRANKLIN H. BARNWELL
JUL26
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FIG. 4. Locomotor activity of a female specimen of:
U. minax collected on July 26, 1966, at Wild
Harbor near Woods Hole, Massachusetts. The crab
was egg-laden at the time o£ collection; the larvae
had hatched by July 31. Circles indicate the predicted times ot high tide at Wild Harbor. The
record is reproduced twice and displaced upward
by one day on the right in order to aid in
visualizing non-24-hr components of activity. The
recording was made in natural illumination. The
bar above the graph indicates the approximate
times of sunrise and sunset at the recording site.
had moved to about 6i/£ hr after the time
of high tide.
A somewhat different phase-relationship
can be denned in Figure 4 by comparing
the midpoint of activity instead of the
onset with the time of high tide. Between
July 26 and Aug. 11, for instance, the onsets
would indicate that the period of the
activity cycle was longer than that of the
tides, but, as can be judged by inspection,
the midpoints do not show such an obvious
difference.
The relative merits of onsets and
midpoints
for determining
phaserelationships have been discussed by
Aschoff (1965). He has suggested that
changes in the mean level of activity may
influence the time in the cycle at which
the onset occurs without altering the timing of the midpoint. It is of interest to
examine the activity pattern in Figure 4
from this viewpoint because the tidal
component does undergo pronounced
changes in level of activity as it scans
across the solar day. It can be seen that
changes in total activity are indeed accompanied by large shifts in the time of
onset in relation to the time of high tide.
The timing of the midpoints does not
appear to be so strongly affected.
The 24-hr character of the change in
level of activity of the tidal rhythm is
apparent in Figure 4. Total activity was
much higher when tide-related periods of
movement occurred between dusk and
dawn than just prior to dark. The only
element of the pattern which recurred
from day to day on a 24-hr basis was a brief
burst of activity at dusk. Clearly the simple
addition of the overt daily component to
the tidal rhythm could not account for the
difference in total activity between afternoon and evening. Instead, the principal expression of the 24-hr component was
through a day-to-day modulation in the
form of the tidal component.
RHYTHMIC SYSTEMS IN FIDDLER CRABS
The studies of locomotor activity have
been extended to tropical species of Uca
on the Pacific and Caribbean shores of
Costa Rica (Barnwell, 1968). Specimens
of U. princeps and U. stylifera were collected at mudflats on the Pacific coast
where the tides are semi-diurnal. The experiments were conducted in March and
April when the crabs were displaying actively in their natural habitat. In the laboratory the crabs exhibited persistent semidiurnal tidal patterns of activity with
distinct 24-hr modulations. An important
component of the patterns was an increase in level of activity when the tidal
peaks occurred between 0700 and 1200.
This period of mid-morning activity recurred at semi-monthly intervals in crabs
maintained either in natural illumination
or in constant darkness. The form of the
rhythm resembled that of the semimonthly cycle of courtship in the closely
related species, U. maracoani (Fig. 1)
(Crane, 1958). The finding of a persistent
semi-monthly rhythm in locomotor activity indicates one level at which a biological timing system could be involved in the
regulation of the semi-monthly cycle of
courtship.
On the Caribbean side, specimens of U.
mordax and U. vocator were collected
from essentially non-tidal colonies on the
banks of rivers a few hundred yards from
their entrance into the sea. The tides on
the coast of this region are mixed, with
an alternation between semi-diurnal and
diurnal forms. When recorded under
natural illumination, the locomotor patterns of these crabs were characterized by
a clearly defined onset of activity at dawn
and a tendency for reduced activity at
night. There was no indication of an
overt tidal rhythm.
In a single transplantation experiment,
11 male specimens of U. mordax were
transferred 110 miles across the continent
from the Caribbean coast to a wire cage
embedded in the intertidal zone of the
Pacific. After an exposure of five days to
the semi-diurnal tides all the crabs were
returned to the laboratory and placed in
577
actographs. At least two of the crabs in
constant darkness exhibited a persistent
semi-diurnal tidal pattern. The phaserelationship between the rhythm and the
Pacific tides was the same as that shown
by crabs of other species which were native to the Pacific. In its major features
the rhythm in the transplanted crabs also
resembled the pattern of locomotor activity which had been recorded in U. mordax
from a region of semi-diurnal tides, the
type locality at Belem, Brazil (Barnwell,
1963; see Barnwell, 1968, for reinterpretation of the pattern).
LOCOMOTOR RHYTHMS IN A REGION OF
DIURNAL TIDES
The studies described to this point have
demonstrated a direct relationship between tidal conditions in the habitat of
the crab and the pattern of its locomotor
and metabolic activities recorded in the
laboratory. Fiddler crabs at Woods Hole
and on the Pacific coast of Costa Rica
tended to exhibit semi-diurnal tidal
rhythms, while crabs from non-tidal rivers
on the Caribbean coast showed a pattern
of activity obviously related to the daynight cycle. In this context it was of considerable interest to examine the rhythms
of locomotor activity in fiddler crabs from
a region of diurnal tides. Such experiments were carried out during the spring
and summer of 1966 with two species of
fiddler crabs collected along the eastern
reaches of Biloxi Bay near Ocean Springs,
Mississippi.
The first species, U. minax, was selected
because it had exhibited persistent,
overt, tidal rhythms at Woods Hole. It
was hoped that equally sharp patterns
from the Mississippi specimens would reveal the manner in which locomotor activity is adjusted to the diurnal tidal cycle. The collection of this species was
made at Old Fort Bayou between 2100
and 2400 on the night of May 5. The
crabs were either sitting in the mouths of
large permanent burrows or feeding on
the surface in proximity to the burrow.
Reproductive activity was disclosed by the
finding of a small male with equal-sized
578
FRANKLIN H. BARNWELL
chelipeds coupled with a larger female at
the water's edge.
The second of the two species proved
to be undescribed, although it is represented in the collections of several museums under the label of U. minax or U.
pugnax. One such instance of mistaken
identify involves the report by Fingerman,
et al. (1958) of a persistent semi-diurnal
tidal rhythm of color-change in U. minax
from Ocean Springs. Specimens of these
crabs had been submitted by Fingerman
to the U. S. National Museum where they
were identified as U. minax. However, a
re-examination of this lot has shown it to
be the same as the undescribed species. In
addition, two visits by the writer to the
collecting site at Ocean Springs described
by Fingerman, et al. (1958) did not yield
specimens of U. minax although large
numbers of the new species were found.
Those colonies of U. minax which were
located on the two visits were on the upper reaches of Biloxi Bay in a region of
very low salinity.
More recently, crabs of the undescribed
species have been identified erroneously
as U. pugnax by Salmon (1967). An examination of Salmon's specimens from
Yankeetown, Florida, has shown them to
be the same as the crabs used in the
present experiments. The latter were obtained in the intertidal zone along the
banks of Simmons Bayou between 1730
and 1830 on May 5. Only males were
collected. Practically all females were
found to be egg-laden.
On May 6 the crabs were transported to
Sebring, Florida, where the experiments
were performed. Recordings of locomotor
activity were made in an air-conditioned
room in which temperature ranged between 23° and 27°C. The animals were
exposed to the natural cycle of daylight
and darkness in front of a shaded eastward-facing window.
In contrast to expectations, the speci-
mens of U. minax showed no indication
of an overt tidal rhythm. The most distinct of six records from this species is
presented in Figure 5A. The overall picture is one of diffuse daily activity which
was initiated at sunrise. There was no
strong nocturnal activity. In lacking a
tidal rhythm and obvious nocturnal activity, this record (Fig. 5A) differs greatly
from that of the Woods Hole specimen
(Fig. 4). However, it should be pointed
out that other records obtained from U.
minax at Woods Hole were characterized
by sharply defined onsets of activity at
dawn during the first 11 or 12 days in the
actographs (Barnwell, 1966, Figs. 1 and
3). Thus, some similarity can be found in
the patterns of activity from the two
widely separated populations of this species.
A 24-hr variation also dominated the
records obtained from nine specimens of
the undescribed species. One of these records is shown in Figure 5B. During the
first four days of recording, activity occurred in short bursts throughout the day
and night. Thereafter a more clear-cut
daily variation emerged. The major
features of the pattern were the initiation
of activity at dawn, apparently slightly in
advance of the specimen of U. minax in
Figure 5A, and a secondary component of
activity centered at about 1000. This record resembles those obtained from, U.
vocator in Costa Rica (Barnwell, 1968).
Experiments in Sebring were terminated on June 25. Surviving crabs of the
undescribed species were transported by
way of Chicago to Woods Hole. Upon
their arrival on July 9, the animals were
placed in actographs in front of a northward-facing window. Records obtained
over nine days again failed to reveal any
signs of an overt tidal rhythm. The crabs
were then divided into two lots. One
group was taken to the Chapoquoit marsh
near Woods Hole and placed in a wire
FIG. 5. Locomotor activity of specimens of (A) V.
minax and (B) an undescribed species of Uca from
Ocean Springs, Mississippi. Conventions are as
in Figure 4. Circles indicate the predicted times of
high tide at Biloxi Bay. Recordings were made in
natural illumination at Sebring, Florida.
579
RHYTHMIC SYSTEMS IN FIDDLER CRABS
MAY 7
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580
FRANKLIN H. BARNWELL
cage embedded in the middle of the intertidal zone. The crabs were left in the cage
for 22 days before being returned to the
actographs on Aug. 12.
The second group of crabs was transferred to a cage implanted in the midst of
the colony of U. minax at Wild Harbor.
Some of the crabs were returned to the
actographs on July 26, but their level of
activity proved to be so low that they
were replaced in the cage at Wild Harbor
on Aug. 3. On Aug. 21, after a minimum
exposure to the tides of at least 26 days,
the crabs were again returned to the laboratory.
Recordings were obtained from six
Mississippi crabs following their exposure
to the semi-diurnal tides. All six crabs
exhibited tide-related activity, with the
three records in Figure 6 providing the
clearest examples. Most evident in each of
the three records is a band of activity
which shifted across the daylight hours at
approximately the rate of the tides. The
phase-relationship between the onset of
activity and the predicted time of high
tide was similar to that recorded in the
activity of U. pugnax, U. pugilator, and
U. minax native to the same marshes
(Barnwell, 1966). In Figure 6C the tidal
component which shifted through the
time of sunrise was unusual in appearing
to possess two bouts of activity during a
single tidal cycle, a major one followed
two hours after its cessation by a minor
one. It can be noted that the record of
Figure 6A was ended on Aug. 22 when
the crab attempted to molt.
The patterns of locomotor activity also
contained 24-hr components. In Figure
6C a short burst of activity recurred daily
at sunrise, while activity was reduced at
sunset. To some extent this variation
reflected the daily rhythm in the freshly
collected crabs (Fig. 5B). In Figure 6B
traces of activity appeared at dawn and
dusk when the bands of tide-related activ-
ity approached these two times of day.
By obscuring or masking tide-related activity, a 24-hr modulation can make it
difficult to determine whether the tidal
rhythm is diurnal or semi-diurnal. Such
was the problem faced by Fingerman in
interpreting the tidal rhythm of colorchange in crabs from Ocean Springs. It may
be recalled that this rhythm can be expressed only during the day phase when the
chromatophoric pigment disperses.
There is similar difficulty in interpreting the records of locomotor activity in
Figure 6. The daytime tide was usually
accompanied by much more activity than
the nightly tide in a 24-hr period. Nevertheless, there were indications that activity could indeed be associated with
the nightly tide. From this it might be
concluded that exposure to the semidiurnal tides of the Massachusetts coast
has induced a persistent semi-diurnal,
rather than a strictly diurnal, tidal rhythm
in the transplanted fiddler crabs.
In comparing the rhythms of locomotor
activity with those of color-change (Fingerman, 1960) in crabs from Ocean
Springs, certain differences in procedure
must be pointed out. Except for one experiment, Fingerman worked with species
different from the ones used here. Also,
his crabs were maintained in darkness,
whereas the recordings of locomotor activity were made in natural illumination.
The most noteworthy difference between
the results of the two studies was that
Fingerman found persistent daily and
tidal rhythms in color-change, while no
obvious tidal rhythm was present in locomotor activity. However, it was demonstrated that a persistent tidal cycle could
be induced in locomotor activity by exposing the crabs to a natural semi-diurnal
tidal cycle. The results of this experiment revealed no inherent limitation on
the capacity of crabs from Ocean Springs
to adjust their persistent patterns of lo-
FIG. 6. Locomotor activity ot three specimens of
the undescribed species of Uca from Ocean Springs,
Mississippi, following their exposure to the
semi-diurnal tides at Woods Hole, Massachusetts.
Circles indicate the predicted times of high tide at
the Chapoquoit marsh and Wild Harbor. The
recordings were made in natural illumination.
581
RHYTHMIC SYSTEMS IN FIDDLER CRABS
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582
FRANKLIN H. BARNWELL
comotor activity to a semi-diurnal tidal
cycle.
Perhaps it should be emphasized that
the undescribed species is not restricted in
its distribution to the region of diurnal
tides. The form occurs eastward as far as
Yankeetown, Florida, where the tide is
mixed and has a pronounced semidiurnal tidal component. The capacity to
time a semi-diurnal tidal rhythm may
have some functional significance in a
region of mixed tides, but it remains to be
seen if this capacity is utilized in adapting the pattern of locomotor activity to
the diuinal tides of the northern Gulf of
Mexico.
CONCLUSIONS
Both observational and experimental
approaches have contributed to our
knowledge of the rhythmic adaptations of
fiddler crabs to the intertidal zone. Historically these two approaches differed in
the order in which they emphasized the
presence of daily and tidal rhythms. Field
workers in the first part of this century
described the obvious relationship between the activity of fiddler crabs and the
tides. Not until the 1950's did prolonged
observations establish the significance of
24-hr and semi-monthly cycles of behavior. In the laboratory, by contrast, attention was called first to the 24-hr rhythm
of color-change (Abramowitz, 1937). The
subsequent analysis of this rhythm by
Brown and his students was regarded as
an important contribution toward the understanding of daily rhythmicity. However, when these workers discovered a tidal
rhythm superimposed on the daily rhythm,
their reports were met with skepticism by many of those working on the
problem of biological clocks. Apparently
there was a reluctance to acknowledge
that an organism could time two slightly
different periodisms in the same process,
since this capacity could not be accounted
for readily by the models which had then
been proposed for the timing mechanism. On the other hand, it can be noted
that ethologists were quick to point out
the correspondence between rhythms of
behavior of fiddler crabs in the field and
the {persistent rhythms recorded in the laboratory (Altevogt, 1957; Crane, 1958).
At that time Crane interpreted the semimonthly pattern of courtship as the result
of the interaction of daily and tidal
rhythms, and she proposed on the basis of
indirect evidence that the pattern was
subject to clock-control.
During the past 10 years it has become
well established that persistent daily,
tidal, and semi-monthly rhythms occur in
various processes of fiddler crabs and other littoral organisms as well. Attention is
now being focused on the ways in which
these persistent rhythms are modified as
adaptations to different tidal environments. It can be expected that continued
research along this line will yield information of double significance. A fuller
understanding of the adaptive roles of
rhythmic systems in littoral organisms
should result, and new information on
the capacities of biological clocks should
be forthcoming. Hopefully this new information will contribute to the development of more comprehensive models for
biological timing systems.
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