Download Some Thermal Requirements of Fiddler Crabs of the Temperate and

AM. ZOOLOGIST, 8:459-469 (1968).
Some Thermal Requirements of Fiddler Crabs of the Temperate and
Tropical Zones and Their Influence on Geographic Distribution
DON CURTIS MILLER
Department of Biological Sciences, Union College, Schenectady, N. Y. 12308,
AND
F. JOHN VERNBERG
Duke University Marine Laboratory, Beaufort, North Carolina 28516
SYNOPSIS. Thermal stress is one environmental parameter that has greatly influenced
the migration of crustaceans from the sea to land. Since a greater number of species of
terrestrial crabs are found in the tropics than in the temperate zone, comparative
studies of the influence of temperature on latitudinally separated populations were
undertaken. Two tropical species, U. rapax and U. thayeri, may occur as far north as
St. Augustine, Florida, or, following a severe winter, may be rare north of Cape
Kennedy. The lethal elfect of the low temperatures recorded during one severe winter
(1957-58) is supported by laboratory studies in which LD^, deaths occurred in 4.5 days
at 10°C for U. rapax acclimated to 18°C. The experiment demonstrates that U.
rapax cannot acclimate to and survive low tempeiatures. This contrasts markedly with
the situation in semi-terrestrial crabs of the temperate zone, which are able to
acclimate to cold.
The distribution of Uca around Cape Cod Bay correlates well with the coastal
hydrographic thermal gradient and supports Passano's suggestion that temperatures
below 20° may be limiting as they inhibit proecdysis in U. pugnax. Such an inhibition
is found experimentally in U. pugilator and in the tropical species, U. rapax. It is
hypothesized that a shift in the thermodynamics of the processes underlying molting
has not occurred in Uca of the temperate zone. The paucity of semi-terrestrial
Brachyura in the temperate zone may be due to the failure of many species to evolve
capacity-adaptations to carry out all requisite life processes at temperatures below 20°,
or the resistance-adaptations necessary to survive the low temperatures of winter.
Considerable knowledge regarding physiological adaptations of Crustacea for
semi-terrestrial life has been obtained
from studies of factors influencing distribution of organisms across the moisture
gradient of the intertidal zone. In contrast to these investigations along the sea
to land gradient, another approach that
serves to demonstrate adaptations to the
rigors of terrestrial life involves comparative studies along a latitudinal gradient,
This is a valuable approach with such
semi-terrestrial Crustacea as the fiddler
crabs. Conditions within their intertidal
habitat differ greatly with latitude, basically as insolation, coastal water temperatures, and tidal regimes vary. Additionali
.•
•
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r r
ly, the genus Uca comprises a large num6
6
"
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b e r
°£ species, most of which are limited
to the tropics. Yet a few species have also
successfully invaded the temperate zone.
is certainly
T h e l a t k u d i n a l
apprOaCh
' '
. '
salient, for as we consider terrestrial
adaptations, we should note that among
brachyurans in general, very few species
h
b e e n successful
i n adapting both to
..
,
.
j
Much of the original work reported in this paper
. ,
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,
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was carried out by the senior author in partial
fulfillment of the requirements for the degree,
Doctor of Philosophy, at Duke University, and
supported by N. S. F. Crams G-5577 and G-8788 to
F. J Vernberg. The authors gratefully acknowledge the marine laboratories which provided
facilities and assistance during this study: The
Research Laboratory, Marine Studios, Marineland;
Entomological Research Center, Florida State
Board of Health, Vero Beach; Institute of Marine
Biology, University of Puerto Rico; Marine Biologia llfe a b o v e
t h e t l d e l m e a
cal Laboratory, Woods Hole; and Duke University
Marine Laboratory.
and
seasonally-fluctuating
459
n d t o
a
w l d e
thermal
re-
460
DON CURTIS MILLER AND F. JOHN VERNBERG
gime. On our East coast, the ghost crab,
Ocypode quadrata, is one of the most terrestrial forms. The principal semiterrestrial brachyurans of the temperate
zone include three species of Uca and two
of Sesarma. Along our Pacific coast also,
the number of semi-terrestrial species in
the temperate zone is small compared to
the number in the tropics. A disparity
between the number of species found in
the tropics and that found in higher latitudes is generally recognized for a variety
of aquatic and terrestrial habitats. Fluctuating thermal conditions appear to be
most responsible for this disparity. Elucidation of the limiting action of latitudinal variables such as temperature is of
interest not only to the biogeographer,
but also to the comparative physiologist.
Some thermal problems and adaptations to be discussed in this paper were
observed during a study of various factors
limiting the geographic distribution of
certain fiddler crabs of the temperate and
tropical zones. Although substrate preference and salinity tolerance were taken
into consideration (to be reported in a
subsequent paper), it was mainly studies
on temperature that provided positive
correlations with observed latitudinal distribution patterns of the crabs.
The geographic distribution of Uca
along the East and Gulf coasts can be
described as follows: The three species of
the temperate zone, U. pugnax, U.
pugilator, and U. minax, reach the
northern extreme of their range in the
vicinity of Cape Cod, Massachusetts. They
are reported to range as far south as
Florida and along the Texas coast (Rathbun, 1918), although only U. pugilator
has continuous distribution around the
southern portion of Florida. Several species of tropical fiddler crabs are also
found on the East coast of Florida: U.
speciosa, U. mordax, U. rapax, and U.
thayeri. The latter three species extend to
the northern third of the coast, and
hence they have a range which overlaps all
three species of the temperate zone.
FIELD STUDIES
Field methods centered upon assessment of the success of populations at stations initially chosen for their apparent
ecological or geographic importance, or
both. Success of populations was measured by estimating density with the direct sampling method employed by Teal
(1958) in his study of Uca. The carapace
of crabs recovered was measured in order
to obtain an expression of density based
on the carapace area per 1/5 m2 sample.
Density values were averaged for each station and the ratio of density : sample area
expressed as a percentage of the 1/5 m2
sample unit. Sampling stations were chosen on the basis of their apparent relatively high population density, because
the purpose of sampling was to determine
maximal densities achieved by the crabs
at a given location. When a relatively
dense burrowing area was located within
a habitat of homogeneous character, samples were taken in a transect across this
area. Environmental data on temperature, salinity, substrate, and vegetational
characteristics were collected at the time
of sampling. In addition, data were collected over longer periods at certain geographically important stations.
Studies near Boundaries of the Geographic Range in Florida, East Coast, 1958-1962
Two fiddlers of the temperate zone and
three tropical species reach the limit of
their respective geographic ranges along
the East coast of Florida between Cape
Kennedy and the border of Georgia. Uca
pugnax and U. minax are quite rare
along the central portion of the coast,
south of Ponce de Leon Inlet. The observed northern limits of the range for
the tropical species are as follows: U. speciosa, just north of Cape Kennedy; U.
rapax, in the vicinity of St. Augustine;
and U. thayeri, north of Jacksonville
Beach. Salmon (1967) found U. mordax
as far north as Daytona Beach.
The population density achieved by
crabs at some of the stations close to the
461
THERMAL REQUIREMENTS OF FIDDLER CRABS
TABLE 1. Maximal density of Uca near the boundaries of its geographic range, Florida East Coast.
Areas with allopatric distribution.
Av. carapace area:
Sample area
Percentage
No . crabs/sample
Av. (range)
Station and habitat
1958
1960
1962
1958
1960
1962
Uca pugnax
Crescent Beach, Short Spartina
5(4-7)
11(8-14)
11(9-13)
4.9
5.8
4.9
14(9-22)
n —5
12 (7-20)
n z= 11
18(17-20)
n= 3
12(8-17)
20(14-31)
n = 10
11(7-17)
n= 4
9(7-11)
n= 5
6.7
85
9.1
5.0
4.2
5.8
Crescent Beach, Salicornia marsh
Johnson's Fish Camp, 4 mi. so.
Marineland, Batis marsh
Mouth of Bulow Creek, Volusia
Co., Batis marsh
Uca minax
Mouth of Bulow Creek, Volusia Co.
Silty Batis and Salicornia marsh
Uca rapax
Pepper Park, Ft. Pierce, clay, sand,
and shell fragments on tidal barren
Uca thayeri
Marineland, low Batis and
yellow mangrove marsh
Pepper Park, Ft. Pierce, muddy
bank with some surface sand
n — 4
7.8
4(2-5)
4(3-7)
n= 5
12 (7-18)
n= 6
9(6-11)
n= 4
3.87
2.8
6.2
7(4-9)
n= 4
5(4-6)
n= 3
limits of their geographic range is
presented in Table 1. For most of these
species, population densities obtained at
stations well within their respective geographic range are also included for comparison (Table 2). Few data are available
for U. minax and U. thayeri, because
they often inhabit creek banks or build
deep and complex burrows where it is difficult to use the direct sampling method. The
densities of U. rapax reported here must be
5.6
7.7
7.4
interpreted with some caution, since Salmon
(1967) recently found that U. mordax occurs
sympatrically with U. rapax between Stewart and Daytona Beach, Florida. These
two species are very similar morphologically but distinct in their sound production and courtship display. None of the
specimens retained from our study at the
stations in question appear to be U. mordax, however.
Populations of U. pugnax and U. mi-
TABLE 2. Maximal density of Uca in North Carolina and Puerto Rico.
Species and habitat
No. samples
No. crabs/sample
Av. (range)
A. Beaufort, North Carolina
U. pugilator—Silty sand beach
9
12
Clean sand beach
12
U. pugnax—Tall Spartina marsh
7
Short Spartina marsh
B. Parguer; Puerto Rico
U. rapax—muddy tidal flat
12
Salt flat, fine shells and clay
10
U. thayeri—Ecotone between black man8
groves and muddy tidal flat
Av. carapace area:
Sample area
41 (27-58)
27 (14-42)
14 (7-20)
13(8-19)
23.4
11(6-15)
15(11-30)
6(3-8)
45
6.7
7.4
4.8
7.7
7.9
462
DON CURTIS MILLER AND F. JOHN VERNBERG
nax were found to inhabit large areas of
the marsh at the stations listed in Table
1, and they achieved high densities in
favorable portions of their habitat. The
densities for U. pugnax in Florida are
comparable to those recorded in the vicinity of Beaufort, North Carolina. Hence,
for the species of the temperate zone
there was reduction neither in the maximal density achieved by the populations
nor in the general size of the area inhabited by the crabs as far south as the Bulow Creek station. This station is only 30
miles, measuring latitudinally, from the
Ponce de Leon Inlet near New Smyrna
Beach, the vicinity of the southern extreme of the range of these crabs.
The tropical crab, U. rapax, was found
as far north as St. Augustine, yet population densities comparable to those observed in Puerto Rico were found only at
Ft. Pierce, some 170 miles, latitudinally,
south of St. Augustine. The populations
of U. rapax found along the northern
portion of the Florida coast were distributed sympatrically, occupying the
narrow portion of the intertidal zone between the high sandy areas inhabited by
U. pugilator, and the lower muddy marsh
of U. pugnax. At several stations between Marineland and Oak Hill, the average carapace area density achieved by
U. rapax ranged from 2.0 to 2.5% of the
sample area.
Temperature is suggested as one major
factor limiting U. rapax in the marshes of
northern Florida. In 1957, Tashian and
Vernberg (1958) found U. rapax near St.
Augustine. Yet the next year, following a
very severe winter, no specimens were
found north of Flagler Beach, and U. rapax was rare in marshes near New
Smyrna Beach. Subsequent studies in 1960
and 1962 showed re-establishment of small
and sparse populations in these areas.
The disappearance of U. rapax in
northern Florida subsequent to 1957 is
thought to be due to winter kill. There
were two prolonged cold spells in this
region during January and February, 1958.
At Marineland, the mean daily air tem-
perature was below 13°C during nearly
two-thirds of this period. This included
four consecutive days in January and
eight in February with a mean temperature below 8°C (unpublished records,
Marine Studios). While comparable data
on temperature are not available for the
Uca habitats at this locality, it is plausible
that temperatures approaching 10° prevailed at the level to which the crabs
burrowed. In the laboratory the median
lethal death point (LD50) at 10° for U.
rapax was found to occur in 4.5 days. This
value is based on a run utilizing 60 crabs
collected in September at Ft. Pierce, Florida, and acclimated to 18° for one week
prior to exposure to 10°.
The suggestion that low winter temperatures limit the northward distribution of
adults of the tropical species, U. rapax,
in Florida is in agreement with findings
of Vernberg and Tashian (1959) on thermal death limits. They observed a marked
difference in survival between U. rapax
and U. pugnax upon exposure to cold. At
7°C the LD.,0 for U. rapax was 30-40 minutes, while mortality for U. pugnax was
very low, even after two weeks. Vernberg
and Tashian concluded that U. rapax is
not capable of acclimating to low thermal
conditions, while U. pugnax can.
This conclusion, based on thermal
tolerance data, was soon substantiated in
the same species by Vernberg (1959), in a
study of the influence of temperature acclimation on O2-consumption of the
whole animal. Figure 1 depicts the genotypic limits of O2-consumption in U. rapax and U. pugnax, using data from coldacclimated (15°) and warm-acclimated
(25°) animals. Of interest to the present
discussion is the inability of the tropical
crab, U. rapax, to make significant metabolic compensation to temperatures of 15°
and below.
In a recently completed study of temperature and salinity tolerances of larval
Uca, Vernberg and Costlow (unpublished) found that first zoeae of U. rapax
are amazingly resistant to low temperature. No mortality occurred among the
THERMAL REQUIREMENTS OF FIDDLER CRABS
463
25% in any experimental group, except
for U. minax at 667<c, when maintained at
36°. It is significant that few differences
were seen between the tolerances of U.
pugnax and U. minnx to these conditions
and that of U. pugilator, even though the
latter species thrives along the southern
coast of Florida. It is apparent that U.
pugnax and U. minax are not restricted to
the northern Florida coasts by limitations
in the adaptations of the adults to high
temperature.
Two studies on laboratory-reared larvae have also failed to show meaningful
differences in the thermal adaptations of
U. pugnax or U. minax compared with
lemperoflure 'c
more southerly species. Considering O2FIG. 1. Genotypic limits o£ O2 consumption of
consumption in first zoea, megalops,
fiddler crabs from the tropical and temperate
and young crabs, Vernberg and Costlow
zones. These limits were determined at various
(1966) observed no clear relationship betemperatures by Vernberg (1959) using data from
ween geographic distribution and metabcold- and warm-acclimated animals. (Reproduced
from Temperature: Its Measurement and Control
olism. Likewise, their recent study of
in Science and Industry, American Institute of Phys- tolerances in larval Uca did not show any
ics, vol. 3, Part 3, J. D. Hardy, Editor, by permisconsistent differences either among the
sion of Reinhold Book Corporation, a subsidiary of
three species of the temperate zone, or
Chapman-Reinhold Inc., 1963, New York).
when these three species were compared
larvae at 5°C after 4 hr o£ exposure, while with the tropical crabs, U. rapax and U.
the LD50 for adult U. rapax is 35 min at thayeri.
7°C. These data suggest that early zoeal
stages of this tropical species may be able Studies Near Boundaries of the Geographto survive in the coastal waters north of ic Range in Massacliuset.ls, 1959
Florida, yet the species does not become
Field studies carried out along the Masestablished because a later stage is less
sachusetts
coast considered only two of
tolerant to low temperatures.
the species in this part of the temperate
The factors limiting the range of the
two crabs of the temperate zone at Ponce zone: U. pugnax and U. pugilator. The
de Leon Inlet have not been determined, third, U. minax, has been collected at a
although the following experiments on West Falmouth marsh (Prosser, Sandeen,
survival at different combinations of tem- personal communications) and recorded
perature and salinity were conducted. from the other side of Buzzards Bay by
The laboratory tests examined the tolerance Rathbun (1918), but was not found by
of all three temperate-zone species to the us. Along the south shore of Cape Cod
combined stress of high temperature (32 to large populations of both U. pugnax and
36°C) and extremes of salinity (6.0 and U. pugilator are found. The densities at&&'/,,). While salinities of these magnitudes tained by U. pugnax at two stations near
are common in the tropics, temperatures at Woods Hole (Table 3) are comparable to
this high level would not plausibly prevail those seen in North Carolina (Table 2).
longer than the daytime 12-hr period of In contrast, very low densities were resolar heating. Yet in the laboratory, even corded for U. pugilator in this area. This
after six days of exposure to the above is most certainly due to the heavy collectstress conditions, mortality did not exceed ing pressure imposed upon these popula-
464
DON CURTIS MILLER AND F. JOHN VERNBERG
tions by workers at the Marine Biological
Laboratory.
On the north side of the Cape, the
distribution reflects the summer atmospheric and hydrographic thermal gradient that exists along the shore line of
Cape Cod Bay. Large populations of both
species, attaining high densities, are
8.
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found in the vicinity of Wellfleet and
First Encounter Beach. Proceeding westward, the populations became smaller
and smaller with respect to the area of
beach or marsh inhabited. U. pugilator
was not found any farther west than
Barnstable Harbor, nor was it located in a
search of protected sandy areas as far
north as Cape Ann. U. pugnax was found
in a marsh near East Sandwich Beach,
inhabiting an area less than 25 m2, yet with
a high density. Very small populations of
this species were also found at three
northern stations along the Massachusetts
mainland: South Duxbury and Brant
Rock, just above Plymouth, and Danvers,
just north of Boston. Except for Wellfleet
and First Encounter Beach, U. pugnax
was found only in uniquely sheltered microhabitats, along tidal creeks some distance inland from the bays. In these areas,
local warming is enhanced during the
summer; the coastal topography protects
the marshes from sea breezes, and the
long circuitous marsh creeks enhance
warming of the flooding tidal waters as
well.
© c*t od
Did
a
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g
o
s
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° 3 S o
u u c e
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The success of fiddler crabs along the
eastern shore of Cape Cod Bay can also
be correlated with local warming, which
is enhanced by shoals that extend offshore
for several miles. In this region, the 15-fathom contour is up to 7 nautical miles off
shore . Considerable atmospheric warming of the shoal waters does occur, according to Bigelow (1927). He observed
the maximum temperatures of shore
waters around Cape Cod Bay to occur
from the last week of July into midAugust. By mid-August the 18° isotherm
enclosed the shore waters all along Massachusetts Bay and down into Cape Cod
Bay as far as Sandwich. Here there is
little shoaling and the 15-fathom contour
lies within 1 to 2 miles off shore. The
remainder of the shore water of Cape Cod
Bay east of Sandwich was above 18°, with
20° being the maximum observed. These
differentials in temperature of the coastal
waters can be validly related to the habitat
temperature of Uca in the summer,
465
THERMAL REQUIREMENTS OF FIDDLER CRABS
TABLE 4. Effect of temperature on molting in eyestalkless Uca.
No. of crabs
(after initial
mortality)
Temp, treatment
%
°C
Molt
Post-treatment
% in pro- % Reecdysis maining
U. pugnax
40
40
40
39
40
Controls
20
15.3
17.6
20.2
0
0
10
21.9
24.6
35.9
97.5
50
0
0
41
52
70
77.5
46.2
27.5
29.5
0
0
87.5
18.0
0
0
92.8
86.7
95
U. rapax
14
15
17
20
15
20.0
22.7
25.1
27.5
70
80
0
20
53
85
80
27.5
0
0
23
33
30
15.2
18.0
20.0
0
3
0
22
22.3
25.0
31.8
54.2
0
0
6.7
73
71
0
0
35.3
47
10
0
Total
% Remaining
%
Molt
Mean duration
of proecdysis
and standard
deviation
(20 days at 29.5°)
0
62.5
0
57.5
0
52.5
0
30.8
0
17.5
62.5
57.5
62.5
66.7
67.5
33.5 -i- 3.63
31.6 •+- 5.08
25.7 -i- 5.35
22.0 •+- 4.92
19.0 ± 5.83
0
—
%
Molt
0
70
(24 days at 27.5°)
21.4
71.4
6.7
73.3
5.9
35.3
10
0
0
0
71.4
73.3
70.6
80
80
35.8
28.0
24.0
14.9
10.0
-t- 2.62
-t- 3.63
-»- 5.13
-+- 4.57
± 2.41
Controls
15
100
V. pugilator
24
91.3
87.9
90
45.8
8.3
46.6
13.3
(22 days at 25°)
21.7
52.2
73.6
76.6
41.7
8.3
9.1
0
0
0
13.3
—
52.2
38.3 -t- 5.23
76.6
76.6
73.5
36.2 •+• 6.75
30.2 •+• 5.11
62.5
23.7 -+- 3.94
17.9 ± 6.63
0
—
Controls
20
25
85
when the burrows are open. It is this
water that will be covering the marshes at
high tide, and hence it contributes directly to the crab's summer thermal regime.
INFLUENCE OF LOW TEMPERATURE ON GROWTH
AND MOLTING
One way in which low temperature
may limit these semi-terrestrial crabs north
of Cape Cod is by its inhibiting effect on
molting. Passano (I960) demonstrated that
low temperature blocked the proecdysial
phase of the molting cycle in U. pugnax.
Molting can normally be induced by removing the eyestalks and hence extirpating
the X-organ-sinus gland complex, which
produces molt-inhibiting hormone (MIH).
In his experiments, at least 70% of the
crabs maintained at 22.2° and above molted
within 23 days, while none of the crabs held
at 20° or below molted during this period.
Temperatures between 15° and 22° considerably extended the duration of proecdysis,
hence delaying molting, and at 15°C and
0
70
below, proecdysis was not initiated. The
onset of proecdysis can be determined by
observing a sharp increase in the rate of
regenerative growth of a walking limb,
which is known to be dependent on proecdysis. This increased rate of growth of
the new limb, which is now influenced by
molting hormone (MH) produced by the
Y-organ, will continue until ecdysis (Bliss,
1960; Passano and Jyssum, 1963).
Passano's experiment has been repeated
using the same species, and two additional ones, U. pugilator and U. rapax. Figure 2 shows the rate, expressed as cumulative percentages, at which molting occurred in each experimental group. Table
4 summarizes the data, which were similar in all three species to those of Passano. There were two differences with U.
pugnax: 10% of the group at 20.2°C
molted during the experimental period,
while none in Passano's 20° group molted.
Also, all of the curves expressing percentage of ecdysis as a function of time were
466
DON CURTIS MILLER AND F. JOHN VERNBERG
smaller, ranging from 13-18 mm in
breadth of carapace. Another variable
affecting molting time in eyestalkless
crabs is their nutritional state.
Should the inhibiting effect of low temperatures on molting play a substantial
shifted to the left about three days,
and the mean duration of proecdysis
was shorter in the present experiment.
These results may reflect differences in
the size of the experimental animals. The
North Carolina U. pugnax were all
00
U. pugnax
80
60
: :
: :
| :
A - 2 4 .6° C
B - 21. 9
C - 20 .2
D- 17. 6
E-
29.5° C
15 3
40
/
/ /
IW y yy
/z'A
A/B.'
20
/
•
/
E
o
-^\\/ 1
/
y
0
Groups -
AH
•
1
10
No.
I
15
20
of Treatment
:
:
•'
/
25
Days
y
1
1
1
t
30
35
40
45
Groups
-
30
35
2A
100
U. p u g i l a t o r
o>
c
i
All
80
25.0°C
a
o 6°
o
*
40
CD
20
E
o
10
2B
15
20
No. of Treatment
25
Days
40
45
4G7
THERMAL REQUIREMENTS OF FIDDLER CRABS
100 .
U. rapax
All
80
Groups
— 27.5° C
60
*
40
>
E
o
20
10
15
No.
of
20
25
Treatment
2C
FIG. 2. Cumulative percentages of molting in Uca
for each temperature-treatment group following removal of eyestalks. All groups in each experiment
role in limiting Uca north of Cape Cod, it
remains speculative whether temperature
is acting on a larval stage or on the
adults. The occurrence of a few small
populations of U. pugnax discontinuously
distributed in sheltered habitats north of
Plymouth suggests that at least during
some years the larvae are able to develop
in these colder bay waters. Also, during
Vernberg and Costlow's recent investigation of larval tolerances, larvae of both
U. pugnax and U. pugilator molted at 15°.
They did not complete development; but
this could be due as much to the rearing
technique as to temperature, since Uca is
very difficult to rear in the laboratory.
DISCUSSION OF THE INFLUENCE OF LOW
TEMPERATURE ON SEMI-TERRESTRIAL
CRUSTACEA
Low temperature appears to limit certain fiddler crabs geographically (1) by
killing adult tropical Uca through extreme winter lows in northern Florida,
30
35
40
45
Days
were maintained at one high temperature following
the 23-day initial period of temperaturetreatment.
and (2) by blocking proecdysis in crabs
north of Cape Cod.
The basic difference between these two
thermal effects is one of intensity. Low
temperature may be ecologically limiting
through (a) immediate lethal inhibiting
effects, which cause death after relatively
short exposure to cold by inhibiting basic
metabolic processes, and (b) delayed lethal
or non-lethal inhibiting effects, which do
not curtail basic metabolic processes, but do
inhibit other systems such as those responsible for growth and reproduction; the organism is affected in direct proportion to the
duration and magnitude of the non-lethal
low.
Adaptations to immediate lethal effects
of temperature are termed resistanceadaptations (Precht, 1958). Acclimation to
cold serves as a resistance-adaptation to
low temperatures in the case of semiterrestrial crabs of the temperate zone,
such as Uca, Pachygrapsus crassipes (Roberts, 1957), and Hemigrapsus oregonensis
and H. nudus (Todd and Dehnel, 1960).
468
DON CURTIS MILLER AND F. JOHN VERNBERG
Non-lethal effects of an environmental
factor have been discussed in detail by F.
E. J. Fry (1947). Using fishes as his principal examples, Fry distinguished four
ways that a non-lethal factor may influence an organism: masking, directing,
controlling, or limiting. According to
Precht's terminology, adaptations of temperature-dependent systems to the nonlethal inhibiting effects of low temperature are called capacity-adaptations. Compensation of metabolic rate to low temperatures following acclimation to cold is
one capacity-adaptation found in many
aquatic poikilotherms of the temperate
zone, including those semi-terrestrial
brachyurans investigated to date.
Various different patterns of compensation to thermal stress occur, not only between species, but also intraspecifically.
Variations within a species may include
differences between ontogenetic stages as
well as between populations, and may often be correlated with the temperatures
of the specific habitats involved.
Vernberg (1959) observed a correlation
between patterns of the metabolism/temperature curves and regional thermal regimes in studies on U. pugnax from North
Carolina and Alligator Harbor, Florida,
and U. rapax from Jamaica. The Alligator
Harbor population, which experiences
high summer temperatures and cold winter conditions, proved to be intermediate
in its metabolic response after acclimation. Cold-acclimated crabs compensated
like the U. pugnax from North Carolina,
but when warm-acclimated they behaved
like U. rapax from Jamaica. An obvious
conclusion is that the specific pattern of
the compensatory adaptation to changes
in temperature is the result of selection
by the local thermal regime.
There are some problems of non-lethal
inhibition by low temperature for which
no adaptation appears to have evolved in
Uca from the temperate zone. Present evidence suggests that the minimal temperature required for molting may be similar
in crabs from the temperate and tropical
zones. Preliminary experiments on low-
temperature inhibition of locomotory activity suggest that species of the temperate
zone have not developed a capacityadaptation to resolve this problem. With
summer animals acclimated to 18°C for
one week, locomotory inhibition occurred
between 11 and 12°C in the three species
of the temperate zone, and between 13
and 14°C in U. rapax and U. thayeri.
Broader comparative studies involving
additional temperature-dependent systems
must be undertaken before a meaningful
generalization can be developed with regards to capacity-adaptations in semiterrestrial Crustacea. Some relevant biological systems include those involved with
growth, metamorphosis of larval stages,
and gametogenesis. If it were true that a
semi-terrestrial group of the temperate
zone, such as Uca, had not evolved many
capacity-adaptations to low temperature,
one would expect them still to require
seasonal periods of tropical-like temperatures in order to carry out certain life
processes. The tropical zone is characterized as having daily minimal air temperatures above 18 to 20°C.
The following air temperatures, which
have primary influence on the thermal
regime of the estuarine intertidal zone,
serve to illustrate similar summer and
differing winter conditions. Consulting U.
S. Weather Bureau data for 1961 from
Morehead City, North Carolina, and
Magueyes Island, Puerto Rico, we find
the ranges for the warmest week were
23.5-32°C at Puerto Rico, and 23-32°C at
North Carolina. The ranges for the
coldest week were 20-28° for Puerto Rico
and —3 to 5.5° in North Carolina. These
ranges represent the averaged daily minimum and maximum temperatures observed during a calendar week. At
Beaufort, North Carolina, the "tropical
season" (with temperatures continually
above 18°) occurs from early June to midSeptember. The duration and intensity of
the "tropical season" diminish proportionately with increasing latitude, and so
does the number of terrestrial and semiterrestrial crabs found along the coast.
THERMAL REQUIREMENTS OF FIDDLER CRABS
Sesarma cinereum is found only as far
north as Chesapeake Bay, and Ocypode
quadrata is rare east of New Jersey, although adults have been reported as far
north as Block Island, Rhode Island
(Rathbun, 1918).
This paper has dealt solely with temperature as a factor influencing the success of semi-terrestrial Crustacea in the
temperate zone. Yet it is well recognized
that the distribution of marine animals is
governed by a complex interaction of
physical and biotic factors, a complex
that is in a constant state of flux. Of
several additional factors that may prove
to be of importance in the adaptation of
these semi-terrestrial forms to the higher
latitudes, a likely one is photoperiod. Semiterrestrial crabs of tropical origin may
require a long photoperiod to trigger or
complete certain life processes. Other
such factors must be considered in order
to understand latitudinal adaptations in
this group of Crustacea.
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