1. No category

Acclimation in Molluscs
Author(s): Earl Segal
Source: American Zoologist, Vol. 1, No. 2 (May, 1961), pp. 235-244
Published by: Oxford University Press
Stable URL: http://www.jstor.org/stable/3881254
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Am. Zoologist, 1:235-244(1961).
IN
ACCLIMATION
MOLLUSCS
Earl Segal
Rice University
The coastal areas of the tropical seas sup?
port a rich and varied invertebrate infauna
These animals live at temand epifauna.
40? C.
Along the
peratures approaching
arctic shores the invertebrate epifauna is extremely poor, but the infauna is as rich and
diverse as in the tropics (Thorson,
1957).
Here, the animals live at temperatures close
to and below 0? C. No species has an arc?
tic to tropic distribution, but many have a
wide latitudinal distribution and thus may
live under extreme temperature conditions.
as contrasted with homioPoikilotherms,
therms, do not regulate their body tempera?
ture; their body temperature changes with
that of the environment.
Biological proc?
esses are determined by temperature, yet
we are presented with the improbable situa?
tion that arctic poikilotherms
metabolize
and grow rapidly in icy waters while tropi?
cal poikilotherms
often metabolize
and
The pos?
grow at a more leisurely pace.
sibility of the existence of compensatory
in poikilotherms
mechanisms
living in
colder and warmer seas, was suggested by
In 1916
August Krogh many years ago.
he
"It
would
be
wrote,
(p. 101),
interesting
to compare the respiratory exchange in such
it would appear
cases, because
unlikely
from a teleological
point of view that it
should differ as much as would be ordinarily implied from the temperature differ?
ence. One would expect that animals liv?
ing at a very low temperature should show
a relatively high standard metabolism
at
that temperature compared with others liv?
ing normally at a high temperature."
We now know that growth rates, respira?
tory rates, and other rate functions of poi?
kilotherms from different environments do
not differ as much as expected from the
temperature differences between the envi?
ronments.
Poikilotherms, which are pasThe studies on Limax flavus were supported bv
NSF Grant G-5943 while I was on the staffof Kan?
sas State Teachers College, Emporia, Kansas.
Temp?C
FIG. 1. Growth rates of shell length of veliger
larvae of the marine gastropod Thais emarginata
from Mount Edgecombe, Alaska, and Big Rock,
California, as a function of temperature. From
Dehnel (1955), by permission of the author and
publisher. "Copyright 1955 by the Universityof
Chicago."
sive conformers to the environmental tem?
changes in
perature, show compensatory
and
rates
in re?
metabolic
rates
growth
in
the
to
encountered
sponse
temperatures
different latitudes (Fig. 1), seasons (Fig. 2),
and microgeographic areas (Fig. 3).
Prior to Krogh's work there had been a
number of studies purporting to show acclimation1 to temperature in poikilotherms,
1 There is no common
agreement on the use of
the terms"acclimation" and "acclimatization." Some
authors make important distinctions between the
terms?although not necessarily the same distinc?
tions?others do not. The term "adaptation" is
generally accepted as the more inclusive term and
thereby acclimation and acclimatization are recog?
nized as a typeof adaptation. Since acclimation and
acclimatization are arbitrary forms of the same
word, I shall refer to any demonstrable compensa?
tory change in an organism as acclimation, to tho
exclusion of acclimatization,qualified by an adjective appropriate to the influenceimposed upon the
organism, e.g. "single factor acclimation," "experi-
(235)
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Earl
236
Segal
no
100
90
80
I9?C
70
? 60
2
(A
h< 50
CD
z
uj 40
1/
\J
9*C
30
20
21
20
JUN
FEB MARAPRMAYJUNJULAUGSEP OCT NOVDEC JANFEB MARAPRMAY
surface
inshore
meanmonthly
for
sea watertemperotures
theyears1953-54
o?'9
?8
uj
cr
5"
or
? 16
5
UJ
14
19-24
9-1414-19
TEMR?C
'
'
i
1_I-1-1-1-1-1
i
i
|
JUL AUGSEP OCT NOVDEC JANFEB MARAPRMAYJUN
TIME IN MONTHS
FIG. 2, Heart rate as a functionof season in the marineintertidalgastropodAcmaea limatula.
?-~"
"
I
but the results of these studies were questionable. The "modern" period began with
the work of Fox, Sparck, and Thorson dur?
ing the 1930's. With the realization of the
mental acclimation," "natural acclimation," "field
acclimation," etc. Similarly, qualifying adjectives
will be used when the phenotypicor genotypicbasis
of the adaptation is in question.
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Acclimation
140itO"
10090
. 80
i 70
? 60
<
mSO
in Molluscs
237
The
environment.
overriding
is that of
animals
faced.
these
by
problem
of
environmental
the
from
severity
escape
Reptiles, like molluscs and other
change.
changing
poikilotherms, cannot regulate their body
temperature by direct physiological activity.
But reptiles do regulate, and thereby es?
Since the
cape, by behavioral adaptations.
due
metabolic
the
of
compensation
portion
the
to
to acclimation is moderate compared
change, ac?
severity of the environmental
role as a
minor
a
climation may play only
Mol?
homeostatic mechanism in reptiles.
to
unable
are
unlike
luscs,
regulate
reptiles,
their body temperature by behavior, thus
from
Of
somples
all of the metabolic compensation
Oic. 17,1953
permitting escape from the severity of environ?
f9
29
24
9
t4
mental change is due to acclimation.
?c
TEMPERATURE
We must here differentiate between ac?
FIG. 3. Heart rate of the gastropod Actnaea limaclimation to the normal temperature range
tula from differentintertidal levels.
as measured by an activity rate (Precht's
or "Capacity adap?
"Leistung-adaptation")
to temperature ex?
acclimation
and
significance o? acclimation to ecology, dis?
tation")
tribution, and evolution, there has been a
tremes as measured by survival (Precht's
manifest growth of interest in this phe?
In those few
"Resistance
adaptation").
nomenon climaxed by the reviews of Bulstudies in which both types of acclimation
lock, Fry, Precht, and Prosser during the
have been examined (Helix pomatia, Mews,
1950*8.
1957; Limax flavus> Segal, 1959; Physa gy~
Bullock (1958), has offered four though t- rina, Beames, unpublished;
Nodilittorina
both
are present
Ohsawa,
provoking problem areas raised by the phe?
1956),
granularis,
nomenon of acclimation:
In general, warm
in the same organism.
1. "The question of the extent and dis?
acclimated animals are relatively heat retribution of ecologically important hosistant and cold sensitive whereas cold ac?
meostatic mechanisms among groups of
climated animals are relatively cold resistThis response is
ant and heat sensitive.
organisms by taxonomic category or by
habitat category.
with
a
in
the
shift
rate-temperature
coupled
2. "The phenotypic versus the genotypic
curve so that cold acclimated animals show
basis for the observed physiological varia higher rate than warm acclimated animals
ation among animal populations.
in the range of intermediate temperatures.
3. "The possible significance of such
However, a common physiological basis for
adap?
tation for biogeography and the deterboth acclimations
remains to be demon?
mination of the limits of breeding and
and
we
continue to regard
should
strated,
of active adult populations.
these as separate processes.
Precht (1958)
4. "The question of mechanisms/*
has further suggested that different mecha?
nisms may be involved in acclimation
to
Unfortunately we are not much nearer
the answers to these questions than we were
extremely high and low temperatures.
20 years ago, in spite of the large numbers
Since my task is to bring together and
of specific examples of acclimation
among
interpret the data on acclimation as dem?
the molluscs and other poikilotherms.
onstrated by the molluscs, I feel it will be
Bartholornew
of value to do so in terms of the aspects of
(1960), clearly stressed the
the phenomenon raised by Bullock.
precarious existence of poikilotherms in a
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Earl
238
Segal
table 1. Distribution of acclimated responseamong gastropods
Measure
Species
Marine
Thais emarginata
Lacuna carinata
Crepidula nummaria
Acmaea limatula
Situation
latitudinal
intertidal,seasonal,ex?
perimental
Littorina littorea
uric acid contentof kidney seasonal
seasonal
Nodilittorinagranulosa extrudingresponse
geographical
experimental
Fresh water
Ancylusfluviatilis
Acroluxuslacustris
seasonal
02 consumption
hot springsvs. river
02 consumption
Physa gyrina
Limnaea stagnalis
02 consumption
experimental
Limnaea stagnalis
excitabilityof isolated foot experimental
Limnaea japonica
growth (larval)
experimental
Terrestrial
Helix pomatia
02 consumption
experimental
Helix pomatia
02 consumption
experimental
Helix pomatia
02 consumption,dehy?
experimental& seasonal
drogenaseactivity
Helix pomatia
Proteolyticactivityof
experimental
stomachjuice
Limax maximus
heart beat (Q10)
seasonal
Limax flavus
02 consumption
experimental
growth (larval)
heartbeat
Authority
Dehnel (1955)
Segal (1956)
Spitzer (1937)
Ohsawa & Tsukuda (1956a)
Ohsawa & Tsukuda (1956b)
Ohsawa (1956)
Berg (1952)
Beames (unpublished data,
Precht (1939)
Benthe (1954)
Imai (1937)
Blazka (1955)
Gelineo & Kolendic (1953)
Kirberger(1953)
Mews (1957)
Crozier& Stier (1924,1926)
Segal (1959 & unpub. data)
table 2. Distribution of acclimated responsesamong pelecypods
Measure
Species
Situation
Authority
Marine
Mytiluscalifornianus
Mytiluscalifornianus
Mytiluscalifornianus
Mytiluscalifornianus
Mytilusedulis
Mytilusedulis
Mytilusedulis
Ostreagigas
Venusmercenaria
Siliqua patula
Mya arenaria
Tivela stultorum
pumping rate
geographical
intertidal
pumpingrate
heartbeat
geographical
shell growth
geographical& intertidal
seasonal
02 consumption
02 consumption(gill tissue) seasonal
02 consumption
geographical
seasonal
ciliaryactivity
02 consumption(tissues) seasonal & geographical
growth
geographical
growth
geographical
growth
geographical
Tables 1, 2, and 3 show the distribution
of the acclimated response among the Mollusca.
Acclimation has been demonstrated
in gastropods, pelecypods, and one species
of amphineuran.
No studies on cephalohave been reported.
pods and scaphopods
Species have been studied from the three
fresh water, and
major habitats?marine,
terrestrial.
heart
Oxygen
consumption,
rate, growth rate, and enzyme activity have
been used to demonstrate acclimation
in
Rao (1953)
Segal et al. (1953)
Pickens (unpub. data)
Dehnel (1956)
Bruce (1926)
Schlieper (1957)
Sparck (1936)
Usuki&Sadaaki (1954)
Hopkins (1946)
Weymouthet al. (1931)
Newcombe (1936)
Coe&Fitch (1950)
response to laboratory and naturally occur?
ring differences in temperature.
Some molluscs do not show acclimation
when subjected to specific tests. However,
the absence of the acclimated response for
a given measure does not preclude its pres?
ence for another measure or for different
conditions. Seasonal acclimation is particu?
Two factors
larly difficult to demonstrate.
may markedly influence the metabolic rate
of the organism and thus obscure the com-
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Acclimation
in Molluscs
239
table 3. Resistance acclimation?Shifting of tolerance levels
Species
Gastropods
Physa gyrina
Helix pomatia
Limax flavus
Nodilittorinagranularis
Nodilittorinagranularis
Littorina littorea
Littorina rudis
Littorina palliata
Patella vulgata
Patella depressa
Patella athletica
Temperature level
high
high (proteolyticactivityof stomach
juice)
low
Authority
Beames (unpublished data)
Mews (1957)
high (seasonal)
high and low (experimental)
Segal (unpublished data)
Ohsawa &Tsukuda (1956a)
Ohsawa (1956)
high (intertidal)
Gowanloch & Hayes (1926)
high (seasonal)
Evans (1948)
Pelecypods
Mytilus edulis
Lasaea rubra
high (gill tissue)
high (intertidal)
Schlieper& Kowalski (1956)
Mortonet al. (1957)
Amphineura
Clavarizona hirtosa
high (intertidal)
Kenny(1958)
In
pensation to the temperature change.
many species the metabolic rate becomes
very high during the breeding season and
the breeding season not infrequently coincides with the warmer environmental
Many other species undergo
temperatures.
a winter rest phase with a decline in the
metabolic rate.
We cannot correlate the ability to acclimate with habitat in the molluscs.
Among
gastropods there are good examples of ac?
climation from marine, fresh water, and
terrestrial habitats.
Not only do molluscs
from all three habitats show acclimation,
they show the same "amount" of acclima?
tion.
This means that we cannot accept
the belief (Scholander
et al., 1953; Fry,
that
of
terrestrial, and
1958)
adaptations
fresh
are
water,
possibly
poikilotherms
related
to
resistance
to
an?
the
the
largely
nual temperature minimum and maximum.
Helix, Limax, Limnaea,
Physa, Ancylus,
and Acroluxus show acclimation of various
activity rates which do not differ in their
order of magnitude
from that shown by
various marine molluscs.
Can we correlate the ability to acclimate
with distribution within a given habitat?
That is, can we show that species with a
wide distribution relative to environmental
temperature (eurythermal) acclimate more
than
species with a narrow distribution
converse?are
The
they
(stenothermal)?
eurythermal because they can acclimate?
here.
may well be the proper question
maintains
that
Schlieper
species in
(1959)
cold deep waters, such as Pinna pectinata
and Avicula hirundo, display little or no
thermal or osmotic compensation, whereas,
species living in surface waters with varying
temperatures and salinities do show such
acclimation.
Schlieper and others have fostered the notion that acclimation is limited
to eurythermal forms. It is true our most
has
of acclimation
important knowledge
come from intraspecific studies of eury?
thermal species (Tables 1, 2, and 3). But,
some stenothermal species have shown sea?
It is
sonal, and laboratory acclimation.
unfortunate that critical tests of Schlieper's
hypothesis have not been carried out. But
the work of Orton (1923), Sparck (1936),
Takatsuki
(1929), Thorson
(1936, 1950),
and Wingfield (1939) has shown that spe?
cies with a northerly distribution have a
faster metabolic rate and heart rate than
southerly distributed species of the same
genus (e.g. Mytilus, from arctic and boreal
waters, and Ostrea, from tropical and north?
ern waters). Developmental
rates may also
show interspecific acclimation since closely
related northern and tropical prosobranch
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240
Earl
Segal
gastropod larvae seem to spend a similar
time in the plankton
(about 3 months).
There is good evidence (Bullock, 1955 and
Thorson, 1956) that the replacing species of
many level-bottom genera of molluscs and
other poikilotherms
are totally or nearly
to the temperatures under which
"adapted"
they live. Scholander et al. (1953), in an
extensive study of tropical and arctic ma?
rine poikilotherms, conclude that there is
meta?
considerable,
although incomplete,
bolic adaptation in the arctic species rela?
tive to the tropical species.
Such interspecific comparisons are diffi?
cult to evaluate.
of rates in
Homeostasis
replacing species of a genus may be an ex?
pression of a genetically fixed adaptation to
habitat
Thus
each species
temperature.
lives only where it can, and, as Thorson
(1957, p. 205) says, ". . . this adaptation allows each genus to be represented in a sea
area by just that species which is able to
carry out the normal functions of the genus
concerned
at the prevailing
conditions."
However, homeostasis of rates may be evi?
dence of a perfectly good ability to accli?
mate even though each species has relatively
narrow infaunal limits.
This leads directly into the second probarea?the
phenotypic versus the genotypic
basis for the interpopulation
differences in
rates
and
thermal
limits. The
physiological
question has meaning only among natural
which have an intertidal or
populations
distribution coinciding with
geographical
temperature differences and thus with dif?
ferences in rate functions.
In laboratory
and seasonal acclimation, the
question has
no meaning; the compensatory
response is
are tests
There
obviously
phenotypic.
available for disclosing the nature of differ?
ences between
natural
populations?sur?
vival polygons, measurements of the
Q10 or
Arrhenius fi for various activities, and, what
is particularly revealing,
reciprocal transplantation and subsequent measurement of
one or more activity rates (see Prosser, 1957,
for a thorough discussion of this
point).
The majority of the latitudinally
separated
of species which show physio?
populations
differences
have not been subjected
logical
90
80
70
i- 40
<
3|c^^o-~<p^_^
24?C.
*<&&&$&
TRANSPLANTSLOWTO HIGH
* ?
HIGH
C0NTR0LS
<
,_ 20
- HIGH
TO LOW
TRANSPLANTS
If <
LOWC0NTR0LS
10
0.4 0.5 0.6 0.7 0.80.9 1.0 1.2 1.4
WET WT. OF SOFT PARTS IN GRAMS
FIG. 4. Relation between heart rate and wet
weight of soft parts of reciprocal transplants and
controls of the gastropod Acmaea limatula 29 days
after transplantation.
to these tests.
I have used the reciprocal
transplantation
technique to demonstrate
a phenotypic temperature effect on heart
rate of intertidal populations
of Acmaea
limatula (Fig. 4 and Segal, 1956). We will
have no idea of the extent of racial differ?
ences between
geographically
separated
populations of a species unless comparable
latitudinal transplantation experiments are
carried out.
Loosanoff and Nomejko
(1951) reciprocally transplanted adult Crassostrea virginica between Virginia and Long Island. The
Virginia oysters failed to spawn in two
the Long
Island
years whereas
oysters
spawned earlier than they normally did in
northern waters. Since the Virginia oysters
normally spawn at 25? C and the tempera?
ture of Long Island Sound failed to reach
25? C during the two years of the study, the
authors concluded
that the northern and
southern populations of C. virginica
represent physiological temperature races. Korringa (1957) has compiled data to show that
there are at least 3 different populations of
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Acclimation
flat oyster, Ostrea edulis,
the European
which differ not only in the temperature
at which release of the larvae can be ob?
served (17?, 20?, and 25? C), but also in
the temperature required for maturation of
that
the gametes.
concluded
Korringa
different
there are several physiologically
races of O. edulis breeding at different temperatures. Commercial oystermen have con?
ducted large scale transplantation
of O.
been
transbut
never
have
edulis,
spat
A
for
racial
better
foundation
planted.
of each
differences within the populations
if
species would certainly be established
both younger and older oysters had been
Stauber (1950) has suggested
transplanted.
that populations
of the oyster drill, Urofrom
and from
Delaware
salpinx cinerea,
be
as
should
considered
Virginia,
physio?
The geographically
logical species.
sepa?
rated populations
have different tempera?
ture thresholds for moving, drilling, and
controlled
trans?
However,
ovipositing.
plantation experiments have not been car?
ried out on Urosalpinx.
Forbes and Crampton (1942) appear to have uncovered physio?
logical races of the fresh water snail Lymnaea palustris from Connecticut and from
New York. These differ in growth rate, fer?
tility, and longevity under similar laboratory conditions. These differences persisted
for three successive generations.
To my
this
has
not
been
followed
knowledge,
study
tests of the natural
up with acclimation
populations.
To illustrate the third problem area?the
limits of the acclimation and the geographi?
cal boundaries of species?I will use my own
work on the pulmonate
gastropod Limax
flavus. I have not found any previous study
on acclimation limits in molluscs.
Fig. 5
shows the rate-temperature curves of oxy?
gen consumption for animals maintained at
2?, 5?, 10?, 20?, and 30? C and measured at
a series of temperatures from -4? to 30? C.
Limax flavus compensates for the difference
in temperature so that, in general, animals
acclimated to the cold have a higher rate
of oxygen consumption
than animals ac?
climated
to the warm when both are
measured at the same temperature.
This is
in Molluscs
400
300
241
FLAVUS
LIMAX
2*;?
*?
ACCL.10?
(1.0gm)
temp.{j*?
30"?1
occlimoted
curvt
rote/temp.
/c<--^
200
s%r,/
gioo
O 80
? 60
-4-2025
JS * s
10
TEMP. ?C.
FIG. 5. Relation between oxygen consumption
and temperature in the slug Limax flavus after
acclimation to a series of temperatures.
the classic picture of acclimation of a rate
function to temperature and need not con?
cern us further. If one connects the points
of
representing the oxygen consumption
animals acclimated to and measured at the
same temperatures
(2?, 5?, 10?, 20?, and
30? C), one has an acclimated rate-tempera?
ture curve. These animals were given sufficient time to become completely acclimated
at each temperature: thus the curve, sup?
posedly, is the more natural curve and
shows what the animals do at their normal
habitat temperatures.
Of course, this is
true
if
we
the
constant tempera?
only
equate
ture of the laboratory with the integration
of the fluctuating temperatures the animals
in the field.
Bullock
experience
(1955,
rate1958) suggests that the acclimated
temperature curve will show (1) a slope
indicating the degree of sensitivity to tem?
perature, (2) a length indicating tempera?
ture range, and (3) a shape at the ends in?
dicating the sharpness of geographic or ecologic limits. The last point is of particular
importance here.
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242
Earl
table 4. Survival of Limax flavus at low temperatures
The limits of acclimation in L. flavus are
2? and 30? C. When measured at temperatures in the physiological
range, animals
kept at 2? and 5? C consume more oxygen
than animals kept at 20? and 30? C. But
animals kept at 10? C show the highest rate
of all.
The lower end of the acclimated
curve is therefore the
rate-temperature
curve for the response of the best adapted
animals (10? C).
It appears as though L.
flavus has an optimal acclimation tempera?
to the exture; the animals acclimated
tremes are not necessarily the ones that do
best at those temperatures.
The limits of
acclimation in L. flavus do not seem to determine the sharpness of transition between
physiological and lethal temperatures and
therefore the sharpness of geographic or
ecologic limits. This point can also be illustrated by survival of L. flavus at low
accli?
temperatures
(Table
4). Animals
mated to 2? and 5? C appear less well
equipped to tolerate low temperatures than
animals acclimated to 10? C.
The last problem area deals with the
mechanism of acclimation.
Acclimation to
temperature has been demonstrated at the
many levels of biological
organization?
whole animal, organ, tissue and cell. The
data is conflicting in that animals which
show metabolic
at the whole
adaptation
Segal
animal or organ level, may or may not show
of tissues and enzyme systems.
adaptation
In some animals the nervous and endocrine
systems appear to play a definite role but
the general belief is that acclimation occurs
at the cellular level. Demonstration of ac?
climation of isolated tissues and of certain
enzyme systems in gastropods and pelecy-
pods (see Hopkins, 1946; Kirberger, 1953;
Mews, 1957; Schlieper, 1957; and Schlieper
and Kowalski, 1956) has contributed to this
belief. This information is all we have on
the mechanism of acclimation in molluscs.
General discussions of the possible mecha?
in poinisms of temperature acclimation
kilotherms may be found in Bullock (1955)
Some of the most chaland Precht (1958).
lenging problems in the study of acclima?
tion center about our understanding of the
nature and site of the mechanisms involved.
Increasingly, the approaches at the cellular
level are more quantitative.
We may soon
be able to determine whether acclimation
depends on shifts in enzyme pathways, syn?
thesis of more enzyme, or changes in the
protein structure of enzymes. We may discover that acclimation
depends on other
at
changes
higher levels of
quantitative
organization.
SUMMARY
Molluscs and other poikilotherms do not
regulate their body temperature yet show
varying degrees of homeostasis of rate func?
tions and shifts in tolerance levels in re?
encountered
sponse to the temperatures
over the seasons, across the latitudes, in dif?
ferent parts of a microgeographic range, and
under experimental
in the
manipulation
This
laboratory.
compensatory response or
acclimation to temperature has been dem?
onstrated in various gastropods and pelecypods and one species of amphineuran from
marine, fresh water, and terrestrial habitats;
the order of magnitude is similar among all
the molluscs.
Most of our knowledge of
acclimation to temperature in molluscs has
come from studies of eurythermal species,
but we do not have sufficient data to permit
us to say that stenothermal species do not or
are less able to acclimate than eurythermal
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Acclimation
in Molluscs
243
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