Download Acclimation of Intertidal Crabs Duke University Marine Laboratory

A M . ZOOLOGIST 9:333-341 (1969).
Acclimation of Intertidal Crabs
F. JOHN- VERNBERG
Duke University Marine Laboratory,
Beaufort, North Carolina 28516
SVXOPSIS. Intertidal crabs are subjected to marked fluctuations in environmental factors. Temperature and salinity influence the distribution of organisms both on a
latitudinal basis and along a subtidal to terrestrial gradient. These factors are operative on all stages of the life history.
Resistance-adaptations. Adult fiddler crabs (genus Uca) from the temperate zone
are more resistant to low temperature than tropical species. Also, the tolerance to
low temperature of crabs from the temperate zone is greatly influenced by thermal
acclimation, i.e.. cold-acclimated crabs are more resistant than warm-acclimated
animals. In contrast, tropical species have limited adaptive ability. At elevated temperatures no consistent difference in the lethal limits of crabs from tropical and
temperate zones is observed. In contrast with the adults, larvae of tropical species
are cold-resistant. However, the larvae of all species tested are more sensitive to
reduced salinities than are the adults.
Capacity-adaptatioyis. Subtidal species of crabs tend to have a lower level of respiratory performance, as measured by various indices, than crabs from the intertidal zone.
The metabolic response of fiddler crabs from the temperate zone is more labile at
low temperature than in species from the tropical zone. At elevated temperature the
reverse response is observed. On an interspecific basis, differences in the metabolictemperature patterns of acclimation of latitudinally separated populations of U. pugilator are observed when based on the hypothetical schemes of Bullock, Precht, and
Prosser.
The intertidal zone has been characterized as a region of environmental instability. Depending in part on the latitude at
which a given intertidal area is found, the
stress-intensity of the various important
components of the environment on the biota will vary significantly. Variation in
temperature will be greater in the temperate zone than in either the tropics or the
polar regions. The salinity of the intertidal
zone may vary to a greater degree than in
the subtidal regions. The time-period of
change also will vary on a temporal basis
as a result of rhythmic phenomena. For
example, there may be semi-daily tidal cycycles, night-day cycles, lunar cycles, and
seasonal cycles. The degree of change
and the significance of this change to the
physiological ecology of organisms will depend on the type of intertidal habitat under study. Sand beaches found along the
shores of harbors and estuaries have a diffSupported in part by Grants G-13954 and G-23570
from the National Science Foundation.
erent set of environmental characteristics
than a sand beach bordering the open
ocean with its unrelenting wave action. In
turn, sand beach intertidal habitats are
markedly different from mudflats or rocky
shores. Organisms characteristic of any one
of these habitats will be subjected to a
different combination of environmental
stresses.
As various components of the environmental complex change, an organism must
be able to tolerate these fluctuations or
move to a more favorable habitat if it is to
survive. The toleration-limits of a population of a species may vary depending
upon a number of variables. One important factor is the previous environmental
history of the organism. For example, a
sample of a population acclimated to low
temperature may survive exposure to low
temperature better than another sample
which had been previously acclimated to
high temperature. However, the toleration-limits of all species may not be shift-
333
334
F. JOHN VERNBERG
ed by acclimation. At present it is not possible to predict with certainty what the
response of a species will be without laboratory experimentation. Not only is it desirable to be able to delineate the tolerationlimits of a species, but also the influence of
the various environmental parameters on
the physiological performance of a species
within its biokinetic zone must be known
in order to understand the basic interaction between the organism and its environment. Animals may be able to survive
(tolerate) a given exposure to an environmental factor, but be unable to compete
successfully with other species because of
poorly developed homeostatic mechanisms
(Croghan, 1961). Hence two main categories of physiologically adaptive phenomena must be studied: (1) resistanceadaptation, the ability to withstand limited exposure to environmental extremes
which are eventually lethal, and (2) capacity-adaptation, alteration in physiological states in response to exposure to an
intensity of an environmental factor (or
factors) which is within the "normal"
range of the species (Precht, 1958).
In this paper the terminology of Prosser
(1958) and Precht (1958) will be used to
describe acclimation in general, and patterns of acclimation to temperature in particular. The present review will deal principally with the ability of certain animals
of the intertidal zone, especially fiddler
crabs (genus Uca) to acclimate to specific
fluctuating environmental factors. Studies
involving most of the stages in the life
history of Uca will be included, since the
environment is acting on all stages.
DISTRIBUTION AND LIFE HISTORY OF Uca
Adult fiddler crabs occupy different
types of habitats in the intertidal zone,
with substrates varying from mud to sand.
Some species are restricted to protected
sand beaches, while others are found in
mangroves or salt marshes. The genus is
widely distributed along the coastal shores
of most regions of the temperate zone and
in all tropical intertidal zones. Along the
east coast of the Americas, species extend
as far north as Massachusetts and as far
south as Argentina, with the greatest
number of species being found in the tropics (Vernberg, 1959a; Vernberg and Vernberg, 1966).
The life history of Uca includes the following stages: (1) The adults live in a
semi-terrestrial habitat and the ovigerous
female carries fertilized eggs on the ventral
surface of her abdomen. (2) Free swimming zoeae hatch from these developing
eggs. Normally there are five distinctive
zoeal stages. (3) The fifth zoeal stage
metamorphoses into a megalopa. The
megalopae undergo further structural reorganization and molt, resulting in young
crabs. The megalopae apparently invade
the intertidal zone and thus represent the
transitional stage between the entirely
aquatic larval mode of life and the semiterrestrial adult stage.
RESISTANCE-ADAPTATION
Tolerance of larvae to temperature and
salinity. The tolerance to various combinations of salinity and temperature of five
species of Uca representing the tropical
and temperate zones was determined. Tropical species were Uca rapax and U. thayeri from Puerto Rico; those of the temperate zone, U. minax, U. pugilator, and U.
pugnax, were from Beaufort, North Carolina.
Ovigerous females were collected and
maintained individually in finger bowls in
the laboratory under conditions of constant temperature (25°C) and salinity (30
%o) in B.O.D. incubators. They were exposed to a controlled photoperiod of 14
hr light—10 hr dark. Only freshly hatched
zoeae were used. During the course of the
experiments to be described below, the
zoeae were fed Artemia and fertilized Arbacia eggs. This diet appeared to be adequate as it proved successful for rearing
these species to at least the megalopa stage
and some to the crab stage. Animals were
used only once.
The tolerances of each species to tem-
335
ACCLIMATION OF CRABS
perature and salinity were determined by
the same procedure. Fifteen to 25 zoeae
were placed in a flask containing sea water
of the desired salinity. Lower salinities
were obtained by diluting sea water with
distilled water and determining the salinity
by standard hydrometric techniques. Each
flask was immersed in a constant temperature bath long enough for the water in the
flask to reach the desired experimental
temperature before the animals were introduced. At the end of the test period the
animals were removed and their condition
noted. An animal was considered dead if,
upon microscopic examination, there was
no visible movement of appendages and if
there was no discernible heart beat. In a
few cases an animal initially was judged
dead by these criteria, but then recovered
with time. Very infrequently an animal
considered alive was dead upon subsequent
examination. Therefore, it was necessary
to make observations both immediately
and after a period of time. From one hatch
of larvae, some zoeae were used for
studies of tolerance to temperature and
salinity and, in almost all cases, another
sample was used for rearing studies. This
last group served as a control to indicate
the viability of the hatch.
Combinations of the following temperatures and salinities were used: salinities,
10%*, 20%«, 35&>, and 50%*; temperatures,
38° and 40°C. These salinity-temperature
combinations may be experienced in the
habitats of these species. Additional observations were made at low temperatures.
During the course of an experiment, flasks
containing zoea were withdrawn at intervals of time to give an estimate of the
duration of exposure necessary to produce
50% mortality. This time, referred to as the
L.D.5O, was calculated for each combination of temperature-salinity and for each
species (Figs. 1, 2).
At both temperatures the greatest survival is at 35#», with the lowest L.D.SO
values at low salinity. No consistent interspecific difference was found which could
be correlated with the biogeographical dis-
1st Zoeal Stage Determined at 33 C.
I
I
35
O
U.
A
0. pufitlitor
I
SALINITY (°/oo)
FIG. 1. Survival of larval fiddler crabs exposed to
different salinities at 38°C. LDM indicates time
required for 50% mortality.
tribution of these species. For example, at
40° the most resistant species and the least
resistant species are tropical forms. As expected, all species lived longer at 38° than
at 40°. At low temperatures, all species
survived at least four hours at 5°C and
larvae of two temperate zone species (£/.
pugnax and U. pugilator) molted when
maintained at 15°C. Interestingly, the latter temperature inhibits molting in adults
(Passano, 1960; Miller and Vernberg, 1968).
Tolerance of adults to temperature and
salinity. The thermal limits of fiddler crabs
reported by various workers have been
summarized recently (Vernberg and Vernberg, 1967). At elevated temperatures no
consistent difference was observed between
fiddler crabs of tropical and temperate
zones. However, interspecific differences
could be correlated with habitat-preferences, i.e., species typically found in
shaded regions were less thermally resistant
than those occupying sand flats or other
habitats exposed to direct sunlight. In contrast, the response to low temperature is
336
F. JOHN VERNBERG
1 s t Zoeal S
(l40*C)
•
I
20
\
I
I
35
50
FIG. 2. Survival of larval fiddler crabs exposed to
different salinities at 40°C. LDM indicates time required for 50% mortality.
clearly correlated with the distributional
limits of fiddler crabs. Species of both the
northern and southern temperate zones are
markedly more resistant to low temperature than are tropical species. For example, at 7° the L.D.5O for tropical species
was less than one hour while species of the
temperate zones survived this temperature
for at least 30 days (Vernberg and Tashian, 1959; Vernberg and Vernberg, 1967).
Of particular importance to life in the
intertidal zone is the ability of species of
the temperate zone to acclimate to a fluctuating environment. Fiddler crabs, irrespective of their zoogeographic affinities
can respond behaviorally to fluctuations in
temperature (Edney, 1961). Animals may
avoid stressful high or low temperatures
by retreating to or remaining in their burrows. However, seasonal changes vary with
latitude and may exert a differential
effect on intertidal crabs from different zoogeographical regions. In the tropics the
annual fluctuation of temperature in air
and water is slight compared with that of
the temperate zone. Two examples may be
cited. Throughout the years, the water
temperature in bays of Puerto Rico ranged
from 26-32°C, while in the harbor at Beaufort, North Carolina, the yearly range was
5-33°C (Coker and Gonzalez, 1960; Pinschmidt, 1963).
Physiological adaptation to this annual
thermal regime has been experimentally
demonstrated for species of the temperate
zone (Vernberg and Tashian, 1959; Vernberg and Vernberg, 1967). When acclimating animals to low temperature and comparing their L.D.5O values with those of
warm-acclimated animals, the cold-acclimated animals of the temperate zone
were significantly more resistant to low
temperature than were warm-acclimated
animals. In contrast, the response of tropical species was little influenced by different
thermal acclimating procedures. This better-developed homeostatic mechanism in
fiddler crabs of the temperate zone has
obvious adaptive advantages in allowing
them to invade and to persist in the intertidal zone of the thermally harsh higher
latitudes. The poleward distribution of
tropical species is restricted by their inability to acclimate to low temperature.
Populations of fiddler crabs are found in
fresh water as well as in the hypersaline
waters of marshes and salt pans. All species
studied to date are capable of hypo- and
hyperosmoregulation. Unlike the larvae,
the adult fiddler crabs are very resistant to
changes in salinity of their external environment (Miller and Vernberg, 1968).
Whereas, the L.D.5O for the first zoeal
stage exposed to 36° and 20 ppt. is about
2.5 days, the adults survive this combination of salinity and temperature at least six
days with a low level of mortality. However, an exception to the general rule that
larvae are more sensitive to environmental
stress than the adult is noted in the thermal response. Larvae of tropical species
can withstand low temperature better than
the adults.
337
ACCLIMATION OF CRABS
TABLE 1. Oxygen consumption and gill area of crabs from different habitats.
Species
Supralittoral Zone
Ocypode quadratus
Sesarma cinerea
Intertidal Zone
Uca pugilator
XJca minax
Panopeus herbstii
Menippe mercenaria
Sublittoral Zone
Callinectes sapidus
Libinia dubia
Rate X
gill area
Eate of Oaeonsump.j
gill tissue**
/il/g/min
Rate X
gill area
2.35
2.21
763.8
1410.0
15.23
15.19
4950
9691
624
513
874
887
2.03
1.28
0.93
0.51
1266.7
656.6
812.8
452.4
9.17
6.21
5.32
5.48
5722
3186
4639
4861
1367
1.14
0.42
1558.4
314.2
5.85
3.57
7997
2670
Gill area*
mmVg
Bate of O»consump. of
whole crab**
325
638
748
* Gray (1957)
•* Vernberg (1956)
CAPACITY-ADAPTATION
Within the zone of compatibility, crabs
of the intertidal zone which can acclimate
to a new environmental complex have an
adaptive advantage over non-acclimating
crabs. Evidence for this is found in metabolic studies where comparisons are made
between closely related species or populations of the same species from different
latitudes or different habitats.
Metabolism of adults: Interspecific comparison. At lower temperatures the temperate zone species, Uca pugnax, has a
more labile metabolic response when acclimated to either high or low temperature
than does the tropical species, U. rapax. In
contrast, the tropical species demonstrates
the greater degree of lability at higher
temperatures (Vernberg, 1959b, 1963). At
one latitude a general correlation between
metabolic rate of both the intact crab and
certain tissues and the habitat of a number
of species was reported (Ayers, 1938;
Vernberg, 1956). Subtidal species tended
to have lower metabolic rates than intertidal or supratidal species. Further, a tendency for a reduction in gill surface with
terrestrialism has been reported (Gray,
1957). When the average rate of respiration is multiplied by the average amount
of gill surface, a trend of the more terrestrial species to have a higher rate of respiratory performance is evident (Table 1).
Two notable exceptions are: (1) Ocypode
which has accessory branchial tufts that
are assumed to have a respiratory function,
and (2) Callinectes, an extremely active
portunid crab.
Metabolism of adults: Intraspecific comparison. Differences between populations
were found in the metabolic-temperature
responses of the tropical fiddler crab, Uca
rapax. However, the adaptive significance
of these differences is not always apparent.
For example, two geographically separated
tropical populations experiencing similar
thermal regimes had different patterns of
response. The one from Salvador, Brazil,
had a higher metabolic rate at temperatures below 28° than animals from Jamaica. Differences between populations found
near the thermal equator and near the
poleward limits of their distribution appear to be adaptive. Uca rapax from middle Florida metabolically acclimate to low
temperature in much the same manner as
species from the temperate zone and reflect
their tropical affinities at higher temperatures (Vernberg, 19596). Populations from
Santos, Brazil, near the southernmost distribution limits of Uca rapax, also show
metabolic adaptation at low temperature
when judged by the classical criterion that
cold-adapted animals consume oxygen at a
faster rate than warm-adapted animals
when measured at a common temperature
(Vernberg and Vernberg, 1966).
-A
Warm-acclimated
200
O
A
O Col d - o c c l i m oted
MASSACHUSETTS
A
A
A A c c l i m a t e d curve
100
NORTH CAROLINA
200 .
200.
FLORIDA
EAST COAST
200
;
A
WEST COAST
100 -
10
15
Temperature
FIG. 3. The rate of O2-consumption of four
populations of Uca pugilator determined at different temperatures. Cold-acclimated animals were
25
°C.
35
maintained at 10°C; warm-acclimated animals at
25°C. See text for explanation of acclimated curve,
339
ACCLIMATION OF CRABS
O
O MASSACHUSETTS
A
A NORTH
CAROLINA
FIG. 4. Comparative metabolic acclimation curves
Cor three populations of Uca pugilator.
In contrast to the preceding example of
metabolic differences of geographically
separated populations of a tropical species,
Uca rapax, the following discussion involves populations of U. pugilator from the
temperate zone. Four populations representing widely different climatic regions
were studied: Cape Cod, Massachusetts;
Beaufort, North Carolina; east coast of
Florida near Miami; and Marco Island on
the west coast of Florida. The rate of
O2-uptake was determined by means of a
modified Wennesland (1951) volumetric
respirometer. The respiratory rate was
acutely determined for cold- and warmacclimated animals over a range of temperature of 5°—35°C. Cold-acclimated animals had been kept at 10°C and warmacclimated at 25°C. In addition, the metabolic-temperature (M-T) curve was determined on animals acclimated to each thermal point (acclimated curve). Only males
in the intermolt stage were used. The general laboratory routine was the same as
described previously (Vernberg and Vernberg, 1966). The data are presented in
Figs. 3 and 4.
Earlier Bullock (1955) proposed a hypothetical metabolic-temperature responsepattern for cold-blooded animals (Fig.
5). Cold-acclimated (CA) animals had
higher metabolic rates at lower temperatures than warm-acclimated (WA) ani-
mals, while at higher temperatures the reverse response was to be expected. However, the M-T response of animals acclimated to each test-temperature (an acclimated curve) would tend to be a composite of the response of the C-A animals
at low temperature and the response of the
W-A animals at high temperature. In the
present study, the patterns of response of
all of the populations of Uca did not conform to this generalized scheme.
The Massachusetts population. At lower
temperatures a classical response was observed in that the C-A animals consumed
oxygen at a faster rate than W-A animals.
However, at elevated temperatures C-A
animals consumed oxygen at a faster rate
than W-A animals. The acclimation curve
was similar to that of the C-A animals at
low temperature but it resembled that of
W-A animals above 25°C which is similar
to the general scheme proposed by Bullock.
The North Carolina population. At 10°
C, W-A animals had the higher metabolic
rate, while at 25° and 30°C the C-A animals
had higher rates. This is the opposite of
the classical response, but the acclimation
curve conformed to the idealized pattern
proposed by Bullock.
The East Coast Florida population. C-A
animals consistently had higher metabolic
rates than W-A animals except at 35°C.
The shape of the acclimation curve was
like that of the one suggested by Bullock.
The West Coast Florida population.
The response of the population from the
west coast differed from that of the popu-
Temperature
FIG. 5. Hypothetical respiration-temperatures
proposed by Bullock (1955).
as
340
F. JOHN VERNBERG
TABLE 2. Patterns of metabolic acclimation to temperature of populations of TTca pugilator from
different geographical regions.
Population
Massachusetts
North Carolina
East Coast Florida
West Coast Florida
Prosser's
classification
Precht's classification
Original temperature of acclimation
10°C
25°C
IIA
•Unclassified
IVA
IIIB
" Type 3—Partial acclimation
Type 4—No acclimation
° Type 5—Inverse acclimation
11
lation of the east coast in that no acclimation was observed at low temperature. At
elevated temperatures the C-A animals
consumed oxygen at a higher rate than
W-A animals.
When plotting the acclimation curves of
three of the populations, distinctive differences can be noted (Fig. 4). At 5°C the
southernmost populations are metabolically depressed more than the two populations of higher latitude. However, unexpectedly at 10° and 15°C, the population
from the middle portion of the geographical range had the lowest rate of O2-uptake. Minor differences were observed at
higher temperature, but no clear cut correlation with latitude. In general, the hypothetical pattern proposed by Bullock did
not clearly apply to all populations of one
species with a wide geographical distribution.
In addition to the hypothetical scheme
proposed by Bullock (1955), two other
methods of respresenting acclimation responses have been suggested (Precht, 1958;
Prosser, 1958). If the metabolic responses
of the four populations are classified using
these two schemes, distinctive populational
differences are noted (Table 2). The
Florida populations showed the most poorly developed ability to acclimate based on
Precht's scheme. Of particular interest is
that the patterns of acclimation of each of
the four populations are different according to both systems of classification.
This emphasizes that generalities cannot
be applied to a species based on the pattern of response of one population. Fur-
thermore, even if acclimation is demonstrated, based on one system of classification, it may not be apparent when using
another method of classification. This does
not invalidate either system but does
demonstrate the necessity for clearly describing the basis for characterizing the acclimatizing ability of a species.
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