AMER. ZOOL., 13:513-528 (1973).
Factors Affecting the Respiration of Intertidal Invertebrates
RICHARD C. NEWELL
Department of Zoology and Comparative Physiology, Queen Mary College,
London El 4NS, England
SYNOPSIS. 'I'he nature and rate of gas exchange in intertidal organisms is variable and is
the product of an extremely complex environmental situation. Such influences may
be grouped into tidal-dependent factors such as the proportion of time spent exposed to air, the magnitude of environmental temperature fluctuations, and the
availability of food. Factors which may be regarded as generally operating independently of tidal level include latitudinal variations in environmental temperature. Superimposed upon such spatial environmental variations are seasonal factors
such as temperature and photoperiod, which impose a temporal cycle upon the
metabolic rate. Finally, there are numerous endogenous factors such as body size,
activity level, and stage of development which profoundly influence the rate of
respiration. It can be shown that some factors, such as aerial or aquatic conditions,
may affect respiration qualitatively. Under aquatic conditions gas exchange is with
the surrounding sea water, but with increasing exposure to air intertidal invertebrates are able to respire aerially and to withstand the water loss associated with
this process. Many are also able to respire anaerobically under conditions of stress.
In contrast, factors such as activity level, body size, nutritional conditions, and exposure temperature affect respiration quantitatively and are often interdependent.
The metabolism of intertidal animals is then endowed with considerable flexibility
between the extremes set by the active and standard rates of respiration. This active rate of respiration is markedly temperature-dependent in most instances, whereas the standard rate, which is characteristic of quiescent animals, is not only lower
but often has a low temperature coefficient. A reduction in respiration conserves
metabolic reserves during periods of stress, and the low temperature coefficient further minimizes depletion of such reserves despite the high environmental temperatures which often prevail during the intertidal period.
INTRODUCTION
Environmental as well as endogenous
factors which influence the oxygen consumption of intertidal organisms have been
studied for many years. Such factors are of
interest partly because physical and chemical conditions on the seashore generally
show a regular gradation from a semi-tcrrestrial environment at high tidal levels
to permanently aquatic conditions on the
lower shore. Equally, there are many
coastal ecosystems which show a latitudinal
transition from temperate to tropical or
even arctic conditions. It is thus possible
to study the effect of both tidal-dependent
factors and latitudinal factors in the respiration of closely related organisms, or
even on the same species. Tidal-dependent
factors include the proportion of time
spent exposed to air, the magnitude of environmental temperature fluctuations, the
availability of food, as well as salinity
stress. Factors which may be regarded as
generally operating independently of tidal
level include latitudinal variations in environmental temperature as well as regular
changes in the availability of oxygen in intertidal deposits ranging from an abundant
supply in coarse deposits to a low level in
estuarine muds. There may also be variations in salinity and nutritional conditions
in estuarine deposits compared with fully
marine ones. Superimposed upon such
spatial environmental variations are seasonal factors such as temperature and photoperiod which impose a temporal cycle on
the metabolic rate. Finally, there are
numerous endogenous factors such as body
size, activity level, and stage of clevelopment which profoundly influence the rate
of respiration.
It is obvious, therefore, that both the
nature and rate of gas exchange in intertidal organisms are likely to be highly
variable and represent the product of an
513
514
RICHARD C. NEWELL
extremely complex environmental situation. Many studies have made valuable
contributions to our understanding of the
influence of such environmental factors on
invertebrate respiration, but nevertheless
have been concerned with only a few of the
possible parameters. Scholander et al.
(1953), for example, made a study of the
influence of short-term exposure temperature and acclimation temperature on the
respiration of a series of latitudinally separated invertebrates and concluded that
adjustment to different environmental temperature regimes was associated with translation of the rate-temperature curves of the
organisms concerned. This results in a uniformity of the respiration rate despite wide
differences in environmental temperature.
Similar temperature-dependent respiration
rates have been noted in many intertidal
animals (Vernberg, 1956; Roberts, 1957a,b;
Dehnel, 1960; Mangum and Sassaman,
1969; Wallace, 1972; Boyclen, 1972; Schick,
1972), and translation of such curves may
indeed be regarded as a general pattern of
compensation amongst intertidal organisms
(Bullock, 1955; Prosser, 1958; Precht, 1958).
An alternative compensatory system is
associated with a rotation of the curves
relating respiration rate to acute temperature change, and this results in low Qlo
values occurring over the temperature
range commonly experienced in the environment. Such low Q lo values are often
approximately 1.2-1.4 and have been demonstrated over some parts of the environmental temperature range in many intertidal organisms including the crab Uca
(Vernberg, 1959), the grass shrimp
Palaemonetes (McFarland and Pickens,
1965), the limpet Patella (Davies, 1966,
1967), in TJttorina and a variety of other
invertebrates (Newell, 1966; Newell and
Northcroft, 1965; 1967; For review, see
Newell, 1969, 1970), in Monodonta (Micallef, 1967; Micallef and Bannister, 1967), in
the sea urchins Eucidaris and Strongylocentrotus (McPherson, 1968; Ulbricht and
Pritchard, 1972), in barnacles (Barnes and
Barnes, 1969), and in the mussel Mytilus
(Newell and Pye, 1970n; Bayne et al., 1973)
as Avell as in some deep-water polychaetes
(Mangum, 1972).
Although the presence of low Q10 values
for the respiration of such intertidal organisms suggests that the oxygen consumption is relatively little affected by the environmental temperature fluctuations associated with the ebb and flow of the tide
(see Newell, 1969, 1970), it is difficult to
establish a clear ecological pattern of variation in such effects. Indeed, in some cases
different temperature effects have been obtained on the same species measured under
different experimental conditions (eg-,
Wallace, 1972; Newell et al., 1972). Even
the effects of temperature alone, therefore,
have yielded very variable reports in the
literature, and it is part of the purpose of
this review to show how such apparently
contradictory results can be reconciled
when the influence of other factors is taken
into account.
TIDAL-DEPENDENT FACTORS
The influence of tidal-dependent factors
on metabolism is complicated by the interdependence of many of the physico-chemical features of the intertidal zone. It is convenient, however, to consider those factors
directly related to aerial or aquatic conditions separately from other parameters
such as activity, temperature, and nutritive
level which are also associated with the
ebb and flow of the tide. In general, the
first category includes factors which affect
respiration of intertidal animals qualitatively, whereas the second group includes
those which principally affect the rate of
respiration and are, thus, quantitative factors.
Qualitative factors
The ebb and flow of the tide has a profound effect on the mechanism of respiration adopted by intertidal animals. Those
living in the lower portion of the shore,
for example, experience almost continuous
immersion, whereas increasing periods of
exposure to air are encountered by animals
living at higher shore levels. Under these
conditions, some intertidal animals can car-
RESPIRATION OF INTERTIDAL INVERTEBRATES
ry out gas exchange not only with the surrounding sea water, but also aerially provided that conditions are moist, and may
resort to anaerobiosis when they become
desiccated (see Newell, 1970).
Air breathing is widespread among intertidal crustaceans. In crabs, for example,
there is in general a progressive reduction
in the importance of gills as sites of gas
exchange in a series characteristic of
aquatic to more terrestrial habitats. Some
crabs such as Uca, Ocypode, and Grapsus
can, however, circulate air through water
which is carried in the gill chambers and
so retain an essentially aquatic method of
gas exchange (Pearse, 1929; Ayers, 1938;
Gray, 1953; for review, see Edney, I960).
Other crustaceans such as the isopod Ligia
oceanica retain the pleopods as the principal site of gas exchange and normally
seek humid conditions in crevices during
the intertidal period (Edney and Spencer,
1955). The barnacles, however, exhibit a
complex series of behavioral responses to
intertidal life and, moreover, show interesting differences between the responses of
species characteristic of the upper and
lower shore respectively. Barnes and Barnes
(1957) showed that intertidal barnacles adjust their behavior in such a way that water
loss is minimized; the cirri are withdrawn
and the valves closed. On the other hand
sublittoral barnacles do not withdraw the
cirri and soon become desiccated. The intertidal barnacles Balanus balanoides and
Chthamahis stellatus are both also able
to air breathe through a small micropylar
opening between the opercular valves; this
is of sufficient diameter to meet the respiratory requirements of the quiescent animal.
Under conditions of prolonged desiccation,
however, the barnacles can close the valves
completely and respire anaerobically, the
accumulated lactic acid being excreted
when the animals are covered by the sea
again (Barnes et al., 1963).
A rather similar sequence of changes
from aerobic gas exchange with the surrounding sea water, followed by aerial
respiration, and finally anaerobiosis, evidently occurs in many molluscs although it
has not been so thoroughly investigated
515
as in barnacles. The mussels Modiolus
demissiis and Mytilus edulis are all able
to breathe both in air and in water (Kuenzler, 1961; Read, 1962; Lent, 1968) and may
also resort to anaerobiosis under conditions
of stress (Dodgson, 1928; Von Brand, 1946).
Many gastropods including the limpet Patella (Davies, 1966, 1967), littorinids (Sandison, 1966; Toulmond, \961a,b; Newell
and Pye, 1971a), and trochids (Micallef,
1966, 1967; Micallef and Bannister, 1967)
are well adapted for aerial respiration.
Deshpande (1957; see also Fretter and Graham, 1962) has shown in a series of trochids
ranging from the lower shore Calliostoma,
through Gibbula cineraria and G. nmbilicalis to the high-level Monodonta, that
there is increasing vascularization of the
mantle, and this is associated with the
ability to maintain high levels of activity
in air (Micallef, 1966; also Newell, 1970).
Indeed, in some intertidal gastropods
aquatic respiration is consistently lower
than aerial respiration, and this is associated with a greater activity of die animals under moist conditions in air (Sandison, 1966; Micallef, 1966, 1967; Micallef and Bannister, 1967). Some of die littorinids are also able to survive for long
periods in the absence of oxygen (Patane\
1946a,£>; 1955), and it is reasonable to assume that most of them are able to close
the operculum. and respire anaerobically
under conditions of stress.
The ability to respire air thus involves
a compromise between the access of air to
the respiratory surface, which is necessary
to maintain aerobic metabolism, and the
evaporative water loss which occurs at high
shore levels. Where the humidity is high,
as under boulders or among algae, aerial
respiration may continue throughout the
intertidal period. In animals which are unable to wholly evade desiccation, however,
the ability to maintain aerial respiration
may be correlated with the tolerance of
water loss. In Patella, for example, as much
as 60% weight loss can be tolerated (Davies,
1969). The shore crab Carcinus maenas,
which is able to air breathe at a comparable rate to that in water (Wallace, 1972;
Newell et al., 1972), is able to survive up
516
RICHARD C. NEWELL
TABLE 1. The general correspondence between sonational position arid the relative importance
of aerial gas exchange in a series of troeliid gastropods.
Species
Monodonta lineata
Gibbula umbilicalis
Gibbula cineraria
Calliostoma zizypliinum
Zonational level
maximum %
exposure to air
Aerial O2
uptake
Aquatic O2
uptake
Gd/g/h/°C)
(/J/g/VC)
75
63
40
10
5.5
5.0
4.0
1.8
5.0
5.5
9.0
10.6
Days to 50%
mortality at
10 C over CaCL,
9.7
3.1
1.5
3.0
The final column shows that the tolerance of desiccation is also related to zonational position
except that G. cineraria, which lives in damp situations, has a low tolerance. Kates of respiration increased linearly with temperature and the increments are expressed as «1 OJ% wet wt/
hr/°C. (Data from Micallef, 1966, 1967.)
to 25% weight loss (Ahsanullah, 1969),
and many prosobranclis can survive up to
20% weight loss (Broekhuysen, 1940; Micallef, 1966; also Newell, 1970). The correspondence between zonational level, the
relative importance of aerial and aquatic
gas exchange, and resistance to desiccation
is shown for a series of trochids in Table
1. It should be emphasized, however, that
these values refer to the routine respiration of the animals and the differences in
rates in air and water mainly reflect an
increased ability to maintain a high activity level under aerial conditions in the upper shore animals (Micallef, 1966, 1967;
Sandison, 1966). Where the level of activity has been standardized as in Littorina
and Carcinus, there is little difference between the oxygen consumption in air and
water (Newell and Pye, 1971a; Wallace,
1972; Newell et al., 1972).
Such organisms thus differ from sublittoral ones not only in their ability to withstand a reduction in their total body fluids
of at least 20% in most cases, but because
they are also able to close the valves or
operculum and resort to anaerobiosis during the unfavorable part of the tidal cycle.
It would therefore not be altogether surprising to find that in these intertidal animals which may regularly undertake anaerobic respiration, there are alternative
metabolic pathways which improve the energy yield under such conditions and so
minimize both the depletion of the metabolic energy reserves and the accumulation of toxic end products of anaerobiosis.
Quantitative factors
Factors which influence the rate of res-
piration of intertidal organisms include activity, body size, exposure temperature, and
nutritive level. Many of such endogenous
and exogenous variables are interdependent and some experimental data are difficult to interpret because of the simultaneous influence of several different parameters. Nevertheless it is possible to select
the results of certain investigations on intertidal organisms which show the likely
influence of such factors independently.
These results may then be used to illustrate the combined effects on the respiration of intertidal animals.
Activity level. The influence of activity
level on respiration rates has been widely
recognized in studies on fishes (see Fry,
1957), but partly owing to the experimental difficulties involved, comparable measurements are scarce for intertidal invertebrates. In general, measurements of the
routine oxygen consumption have been
made although there are now some data
available for both inactive and active animals. In Littorina and several other invertebrates, for example, periods of activity
are associated with higher levels of oxygen consumption than during quiescence,
and this allows the separation of an "active" from a "standard (or quiescent)" rate
of respiration (Newell and Northcroft, 1965,
1967; Newell and Pye, 1970a, I97\a,b; for
review, see Newell, 1969, 1970). Other organisms, such as the shore crab Carcinus,
may remain quiescent in a respirometer
so that the rate of oxygen consumption approaches that of the standard rate (Wallace, 1972; Newell et al., 1972), while
quiescence can be induced in the shrimp
Crangon vrrfgaris by the provision of a
517
RESPIRATION OF INTERTIDAL INVERTEBRATES
suitable substratum (Hagerman, 1970).
The activity level can be more easily
quantified in those intertidal organisms
which either irrigate the body, as in polychaetes and bivalves, or are mobile as in
many crustaceans. Halcrow and Boyd
(1967), for example, measured the oxygen
consumption of the amphipod Gammarus
oceanicus in relation to swimming activity
and were thus able to measure the active
rate and to estimate the standard rate from
the graphs relating oxygen consumption
and activity. McFarland and Pickens
(1965), in an important study on the effect
of a variety of factors on the respiration of
the grass shrimp Palaemonetes vulgaris,
were able to measure both the standard
rate and the rate of oxygen consumption
of shrimps swimming against a current of
water. In this way the oxygen consumption at a variety of swimming speeds could
be measured much as has been accomplished in fishes. Mangum and Sassaman
(1969) have synchronously recorded the activity and oxygen consumption of the polychaete Diopatra cuprea, although they were
able to record rates for fully active and
quiescent animals only. More recently, a
detailed series of studies have been made
on the influence of activity and other factors on the respiration of the mussel Mytilus edulis by Thompson and Bayne
(1972), Widdows (1972), and Bayne et al.
(1973). They showed that mussels normally irrigate and consume oxygen at a "routine rate," but that the filtration rate can
be increased to an "active rate" following
presentation of suitable food such as a suspension of the flagellate Tetraselmis.
The relationship between ventilation
rate and oxygen consumption in a specimen of Mytilus at 15 C is shown in Figure
1 (based on Bayne et al., 1973). It is evident that in this animal activity is proportional to the logarithm of the oxygen consumption, although in other studies on
Mytilus (Thompson and Bayne, 1972) and
in Gammarus oceanicus activity is related
directly to oxygen consumption. These latter data resemble those obtained in many
studies on fishes (Spoor, 1946; Fry and
Hart, 1948; Beamish and Mookherjii,
0-8
1
0-6 _-4
-
1
1
1
Active
I
O 0-4
^
Standard
z
o
MYTILUS
0
1
10
VENTILATION
1
20
EDULIS
30
1
40
RATE, ML MIN" 1
FIG. 1. Graph showing the relationship between
irrigation rate (ml water/min) and oxygen consumption (ml O2/g/dry wt/hr) in a 1.0 g/specimen
of Mytilus edulis at 15 C. (Based on Bayne et al.,
1973.)
1964; Muir et al., 1965; Muir and Niimi,
1972) and may be more typical of the results to be anticipated in intertidal invertebrates. The result of these differences in
the rate of respiration of active and quiescent animals is that regression lines relating active and standard metabolism to
body size are different in level. The rate
of oxygen consumption of routinely active
animals, however, is intermediate between
these two values and usually shows considerable scatter about the regression line, reflecting individual variations in activity
level.
Figure 2/4 shows the active and standard
rates of respiration of the fish Kuhlia at
23 C plotted as a function of body weight;
similar data for the intertidal gastropod
Littorina littorea at 20 C are shown in Figure 2B (data from Muir and Niimi, 1972;
Newell and Roy, unpublished). Much the
same type of relationship has been demonstrated in the mussel Mytilus edulis
(Thompson and Bayne, 1972) as well as in
the shore crab Carcinus maenas (Wallace,
1972) and must certainly apply to most
marine organisms. The difference in level
between the active and standard rates defines the "scope for activity" of the organism concerned (see Fry, 1957), and this
varies according to the work performed
during locomotory or irrigatory activity.
This value is difficult to estimate by mere
inspection of the experimental organism
concerned. The energetic cost of activity
518
RICHARD C. NEWELL
1
1
A.
I
I
I
1.. B.
KUHLIA
20 Active
.
.yA'x"
LITTORINA
o "
i .0
i
8
s-
4
Standard
Standard
10
20
WET
1
I I I
30
40 50 60
WEIGHT, G
1
80
2
io
DRY
20
WEIGHT. MG
FIG. 2. Graphs showing the relationship between
oxygen consumption and body weight in (A) the
fish Kuhlia sandvicensis at 23 C and (B) the winkle
Liltorina littorea at 20 C. (Data from Muir and
Niimi, 1972; Newell and Roy, unpublished.)
may, for example, be as high in a relatively sluggish animal which during locomotion moves a shell many times its own tissue weight as in a fish or in a pumping bivalve. Comparisons between the scope for
activity for different organisms (Newell,
1970; Wallace, 1972; Boyden, 1972) have,
therefore, little quantitative significance
unless expressed in terms of work performed during activity. The scope for activity may also vary according to a number
of other factors, including temperature
and nutritional conditions, some of which
are discussed in more detail below.
Body size. Body size is the second important endogenous factor which affects the
respiration of animals, and it has been
fully demonstrated in a wide variety of
organisms that the line relating log metabolism to log body weight has a slope of
approximately 0.75 (for reviews, see Zeuthen, 1953; Hemmingsen, 1960). In many
instances the respiration of intertidal organisms of a wide variety of sizes has been
measured so that variations in the level or
slope of the regression lines give an indication of the influence of external conditions on metabolism. This approach has
been used in studies on the crabs Pacliy-
grapsus (Roberts, 1957a,£>), Uca (Vernberg,
1959), Hemigrapsus (Dehnel, 1960), and
Carcinus (Wallace, 1972; Newell et al.,
1972), as well as in the shrimp Palaemonetes (McFarland and Pickens, 1965) and
barnacles (Barnes and Barnes, 1969). It has
also proved valuable in studies of many
other organisms including bivalves (Read,
1962; Kennedy and Mihursky, 1972), the
limpet Patella (Davies, 1966), the winkle
Liltorina (Newell and Northcroft, 1967;
Newell and Pye, 1970a, \91\a,b; Toulmond, 1967a,b), and the cockle Cerastoderma (Boyden, 1972).
Although these studies have in general
confirmed the overall relationship between
log metabolism and log body weight, there
are many instances where the slope b of
the regression line varies according to external conditions such as temperature. The
occurrence of this variation in the earlier
literature has been reviewed by Rao and
Bullock (1954) and has since been confirmed in Uca by Vernberg (1959). More
recently, similar effects have been noted in
the slug Avion by Roy (1963, 1969), in
barnacles (Barnes and Barnes, 1969), and
in the winkle Littorina (Toulmond,
1967 a,b; Xewell and Pye, 1971«; Newell
519
RESPIRATION OF INTERTIDAL INVERTEBRATES
and Roy, unpublished). The result of this,
as has been recognized by Rao and Bullock (1954) and Vernberg (1959), is that
temperature or other external conditions
may have a different effect on large and
small individuals of the same species.
Unfortunately, data for the respiration
of intertidal animals showing routine levels of activity are usually so scattered that
the significance of differences in the slope
b is very difficult to establish. Davies
(1966, 1967), for example, found no significant difference between the values of b
for the respiration of the limpet Patella
under various experimental conditions and
used a mean common regression coefficient
in an interpretation of his data. A similar
approach has been used by Sandison
(1966) on gastropods and by Wallace
(1972) on Carcinus. Although the use of a
mean value for the regression coefficient is
undoubtedly valid, it is to be hoped that
a strict control of activity in the respirometer may lead to a reduction of the variability of the data and this may in turn aid
the analysis of differences in the slopes of
lines relating log metabolism to log body
weight. Roy (1969) used a slightly different
approach in an interpretation of data on
respiration of the slug Arion circumscriptus. He used multiple regression analysis
on a large number of observations of metabolism under a variety of experimental
conditions and then employed the statistical model obtained to predict the effect of
external factors on metabolism. We have
recently used this technique to analyze the
influence of exposure temperature on the
relationship between body size and metabolism in Littorina littorea (Newell and
Roy, unpublished). The results for active
and inactive animals at a variety of exposure temperatures are shown in Figure 3.
It is evident that the statistical model
predicts that the value of the slope b varies
directly with exposure temperature and in
this respect resembles the data cited by Rao
and Bullock (1954) for Talorchestia from
work by Edwards and Trving (1943). On
the other hand, it is the reverse of the relationship found in Uca (Vernberg, 1959),
Arion (Roy, 1969), and barnacles (Barnes
I . 375.b59-
2-25
210
1-95
1-80
1-65
3
120
LOG
DRY
WEIGHT, MG
FIG. 3. Graphs showing the influence o£ short-term
exposure temperature (Tc) on the relationship between metabolism and body size in Littorina littorea. Values for the slope (6) are also shown.
(Data from Newell and Roy, unpublished.)
and Barnes, 1969) in which the value of b
was inversely correlated with exposure temperature. Further work is clearly necessary
to establish whether this pattern of variation about the common regression coefficient established in interspecific studies
(see Zeuthen, 1953; Hemmingsen, I960) is
of general occurrence. The data available
at present, however, suggest that variation
in the relationship between metabolism
and body size according to exogenous factors is not always in the same direction
and may complicate the interpretation of
the influence of environmental factors such
as temperature on respiration (Newell et
al., 1972).
Nutritional conditions. The influence of
nutritional conditions has been implicated
in many studies on the respiration of intertidal animals. Roberts (19576) showed
that the rate of oxygen consumption of the
crab Pachygrapsus falls to approximately
60% of the initial rate following 23 days
starvation at 16 C, although the most rapid
decline occurred in the first 7 days. Compa-
520
RICHARD C. NEWELL
rable results have been obtained on Uca
by Vernberg (1959) who found that the
major decline in respiration occurred within 7 days. Much the same type of response
has been demonstrated in the crab Paratelphusa by Rajabi (1961) who showed in
addition that when starvation is continued
for 21 days, there is a greater decline in
the respiration of small crabs than large
ones. A similar decline in oxygen consumption following starvation has been noted in
the fishes Gadus morhua (Saunders, 1963)
and in Kuhlia (Muir and Niimi, 1972). A
detailed study of the influence of starvation on metabolism has also been made by
Barnes et al. (1963) who worked on the
barnacle Balarms halanoides. They showed
that carbohydrate reserves are utilized
first, but that after these have fallen to approximately 10% of the body weight, protein and lipids are used as metabolic substrates. Similar studies on the effects of starvation and seasonal influences on the major biochemical components of intertidal
animals have been made by Neiland and
Scheer (1953) who worked on Hemigrapsus, Steeves (1963) on the isopod Lirceus,
Emerson and Duerr (1967) on Littorina,
Stickle and Duerr (1970) on Thais, and
Zwann and Zandee (1972) on Mytilus (see
also Giese, 1966).
There have also been a number of recent studies which show that starvation not
only influences the rate of respiration of
intertidal animals, but may also play an
important part in controlling the scope for
activity. Hagerman (1970) has shown that
the active rate of respiration of the shrimp
Crangon vulgaris declines over a period of
8 days starvation at 10 C but that the standard rate of quiescent animals is unaltered. That is, starvation affects the scope
for activity so that starved animals are
usually quiescent. Starvation may also have
a significant influence on the temperature
relationships of metabolism in such animals. Davies (1966, 1967) showed that in
the limpet Patella, individuals from high
shore levels or bare rock surfaces had not
only a lower respiration rate but also were
less affected by temperature than animals
from the lower shore or areas rich in algae.
This suggested that nutritional factors may
play a part in determining the rate-temperature relationships of Patella. Again,
Barnes et al. (1963) have shown that the
temperature coefficient for the molting frequency of Balanus balanoides varies according to the substrate being utilized. The
Qi0 value is approximately 2.0 in well-fed
barnacles using carbohydrate as a substrate
but falls to 1.0 when protein and lipid are
being used.
We have not detected any significant difference between either the active or the
standard rate of respiration of Littorina
following starvation for 3 weeks at 7 C
(Newell and Pye, 1971a), although the level and temperature relationships of the metabolism of subcellular preparations are
markedly dependent upon added substrate
concentration (Newell and Pye, \91lb,c).
More recently, however, Thompson and
Bayne (1972) and Bayne et al. (1973) have
shown that in Mytilus edulis there is a
decline in the active rate of respiration towards routine levels after approximately
5 days of starvation and that further starvation results in a fall in the respiration
rate towards the standard rate. Their data
thus support those for Crangon (Hagerman, 1970) and suggest that starvation in
these animals acts principally upon the level of activity which can be maintained.
The influence of starvation on the respiration of the mussel Mylilus edulis and the
shrimp Crangon vulgaris is shown in Figure 4.
There is also a definite influence of starvation on the respiration rate of Carcinus
although at present it is not altogether
clear whether this is due to a suppression
of activity from a routine to a standard
rate, or whether the standard rate itself is
capable of suppression. Storage of crabs in
the laboratory at 15 C results in a progressive suppression of the respiration over a
period of 3 weeks compared with fully fed
crabs. Further, the influence of starvation
on the respiration of small crabs was greater than in large crabs (Newell et al., 1972;
Marsden et al., 1973). In this respect the
data support those of Rajabi (1961) for the
freshwater crab Paratelphusa, and suggest
521
RESPIRATION OF INTERTIDAL INVERTEBRATES
~i
A.
1
1
—T
r
CRANGON
—1
—T
Active
-
V
1
1
1
1
1
B.
1
MYTIIUS
—1
!
•I
•
-
\
o
•' --
i
iI
- 1
1Standard
i
I
Routin
I'
_
FED
I
DAYS
AFTER
CAPTURE
FIG. 4. Graphs showing the influence of starvation
and feeding on the oxygen consumption of (^4) a
shrimp Crangon vulgaris and (B) a mussel Mytilus
edulis. Data for Crangon showing rate of oxygen
consumption (mm3 (X/g/wet wt/hr) of active and
inactive animals during starvation at 10 C for 9
days (after Hagerman, 1970). Data for Mytilus
showing rate of oxygen consumption (ml O2/g/dry
wt/hr) of animals which had been starved for two
weeks at 15 C and then fed. Note that the rate rapidly increased to the active rate of oxygen consumption but later declined to a routine rate.
(Based on Thompson and Bayne, 1972.)
that nutritional factors may be implicated
not only in controlling the level of metabolism but also in influencing the relationship between body size and metabolism.
Such factors are clearly of importance when
one considers that many studies are made
on organisms which have been starved for
a variable time during storage in the laboratory. They may also have some significance in an interpretation of seasonal
cycles in the metabolism of marine invertebrates which are commonly subjected to
marked variations in food availability at
different times of the year.
Exposure temperature. The influence of
temperature on the respiration of intertidal organisms has received more attention
than other environmental factors perhaps
partly because it is an obvious parameter
which varies with shore level as well as
with latitude and season. These last two
categories involve essentially long-term differences in environmental temperature,
whereas alterations in exposure temperature associated with shore level involve
semi-diurnal fluctuations in external conditions. It is, therefore, useful to separate
such tidal-dependent temperature fluctuations from seasonal and latitudinal
changes in the thermal regime.
As has been mentioned above, many of
the earlier studies on the respiration of
marine invertebrates have been concerned
with routine metabolism. There are, therefore, many patterns of variation in the
metabolic response of such animals to temperature, and this reflects in part the different effects of temperature on factors such
as activity level, body size, and nutritional
state of the organisms concerned. The first
and perhaps the most important single factor which affects the temperature relationships of respiration in intertidal organisms
is activity. The rate of activity, and consequently the active rate of respiration, nearly always increase logarithmically with
temperature with a Q]0 of approximately
2.0 (see Schlieper, 1952; Prosser and Brown,
1961; Newell, 1970). Such processes include
ciliary activity in mussels (Gray, 1923;
Schlieper et al., 1958), cirral activity in barnacles (Southward, 1964; Ritz and Foster,
1968), radular activity of periwinkles (Newell et al., 1971&), and the heart rates of
many intertidal animals (see Maynard,
I960; also Pickens, 1965; Ahsanullah and
Newell, 1971). It is not surprising to find,
therefore, that in most instances where the
experimental animal is either fully active
or showing a routine level of activity, that
the respiration rate is essentially dependent upon temperature (see Fig. 6).
In contrast, a variety of different temperature effects have been reported for the
522
RICHARD C. NEWELL
respiration of quiescent intertidal invertebrates. Such relationships vary from temperature dependence throughout the range
of thermal tolerance of the organism concerned to rate-temperature curves which
show low Q10 values over at least part of
the environmental temperature range (see
above). The occurrence of such regions of
temperature insensitivity has been reviewed
by Bullock (1955), Vernberg (1959), Newell (1969, 1970), and Boyden (1972) and in
general appears to be confined to organisms subjected to regular cyclical temperature fluctuations such as are associated with
the ebb and flow of the tide. Recently, for
example, Ulbricht and Pritchard (1972)
have shown that in the intertidal sea urchin Strongylocentrotus purpuratus the
metabolic rate was essentially independent
of temperature between 12-21 C, whereas
the subtidal S. francisccmus has a high value
for the Q10 throughout the environmental
temperature range. Similarly in the intertidal winkle Littorina littorea and in the
barnacles Balanus balanoides and Chthamalus stellatus, regions of thermal independence occur when the respiration of
quiescent animals is plotted against temperature (Newell, 1969; Barnes and Barnes,
1969). Again, in the mussel Mytilus edulis
the oxygen consumption of quiescent animals has a low Q,o value, whereas the respiration of routinely active animals is
markedly dependent upon temperature. In
this animal, however, the fully active rate
of respiration also has a rather low temperature coefficient as in the standard rate
(Widdows, 1972; Bayne et al., 1973). The
standard rate of respiration of the polychaete Diopatra cuprea, which normally
lives buried beneath the surface of deposits and, hence, experiences little temperature fluctuation is, however, dependent
upon temperature (Mangum and Sassaman,
1969). There, thus, appears to be an ecological pattern in the occurrence of such
temperature-insensitive metabolism. The
occurrence and possible biochemical mechanisms which might account for this phenomenon in intertidal and other organisms
have been discussed elsewhere (Somero,
1969; Newell, 1970, 1973; Newell and Pye,
I971fo,c; Hochachka and Somero, 1971; Hochachka, 1973).
One of the problems with the interpretation of such temperature effects in ecological terms is that there are many examples of intertidal animals which do not,
apparently, show extensive regions of temperature independence even though the organism may be subjected to environmental
temperature fluctuations. Equally, Mangum (1972) has shown that in the subtidal
polychaete Hyalinoecia respiration is independent of temperature over a wide range
even though the animal lives in a thermally stable environment. A possible explanation of this anomaly is suggested by the
work of Davies (1966, 1967) on Patella. As
mentioned above, his data showed that the
Q in for respiration varies not only inversely with tidal level but also according to the
availability of food.
We have investigated the relationship
between nutritional factors and the temperature dependence of respiration in the
shore crab Carcinus maenas (Marsden et al.,
1973). Figure 5 shows the rate-temperature
curves for 4-g dry weight specimens which
had been stored at 15 C for up to 20 days.
It is clear that starvation resulted not only
in a suppression of the respiration after one
week, but that after 20 days the metabolism was much less dependent upon temperature. These data suggest, then, that the
temperature dependence of the metabolism
of subtidal animals compared with those
of the upper shore may be associated with
the availability of food. Although some intertidal animals can compensate for the reduced feeding time associated with the upper shore (Morton et al., 1957; Newell et
al., 1971 b), such examples are comparatively rare (see J0rgensen, 1966; Newell, 1970).
Indeed, even if compensation in the rate
of feeding were complete, it has not been
established that food availability is the
same on the upper shore compared with
lower tidal levels. The occurrence of suppressed rates of respiration, with their associated low Q ln values in a wide variety
of animals of the upper shore (see above)
may thus represent a means by which energy is conserved despite the rise in tern-
RESPIRATION OF INTERTIDAL INVERTEBRATES
1
1
7-9
-8
1
DAYS
1
1
/
. - .
\
J
,
-
Starved
\
-
~
\
^
•6
Fed
1
^ 1-2 X
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Fed
~
DAYS
S 10
^-°
-
Slmved
/
/
/
i
1
20
1
1
DAYS
EXPOSURE
TEMPERATURE.
C
FIG. 5. Graphs showing the effect of temperature
on the respiration of crabs which have been starved
or fed in the laboratory at 15 C for up to 20 days.
One group of crabs (closed symbols) fed with fish
and the other (open symbols) starved. Note that
after 14-16 days the rate-temperature curve for
starved crabs becomes suppressed and less dependent upon temperature than for the fully-fed crabs.
Data for a 4.0-gram dry weight animal. (From
Marsden et al., 1973.)
perature which occurs during the intertidal
period. Equally, the sporadic occurrence of
low Q lo values in subtidal organisms may
reflect the presence of low metabolic substrates induced by starvation or metabolic
stress. When the tide covers the intertidal
animals, however, substrate levels may be
enhanced and the higher, temperature-dependent rate characteristic of active animals is established (Newell and Pye,
1971fe,r; Newell, 1973).
LATITUDINAL FACTORS
Latitudinal factors which affect the respiration of marine organisms are principally associated with long-term changes in
the environmental temperature regime. As
523
has been mentioned above, there are many
examples of compensatory processes by
which the respiration rate is maintained
at a uniform level despite wide variations
in external conditions such as salinity and
temperature. The characteristics of such acclimatory processes have been reviewed by
Bullock (1955), Prossor (1955, 1958), and
Precht (1958), and several different patterns
of compensation have been found to occur.
In the case of acclimation in response to
latitudinal or seasonal changes in environmental temperature, however, translation
of the rate-temperature curve to the right
following warm acclimation is a common
pattern of adjustment. A shift in the ratetemperature curves for activity in barnacles
in response to warm acclimation is well
established (Southward, 1964; Crisp and
Ritz, 1967a,fo; Ritz and Foster, 1968) and
occurs also in the isolated gills of intertidal
bivalves (Vernberg et al., 1963). The result
is that comparable-sized individuals of any
one species with a wide geographical range
show similar levels of activity and metabolism at the northern and southern limits
of their distribution (Mayer, 1914; Scholander et al., 1953).
The rates of oxygen consumption of active and quiescent Littorina taken from
high levels on the shore at three different
times of the year are shown in Figure 6.
From this it is evident that the rate of respiration of active animals was temperature
dependent but that by translation of the
rate-temperature curve the respiration was
maintained between 1.8 and 2.2 /xl O2/mg
protein/hr in a specimen of 30 mg dry protein weight despite a variation in environmental temperature from 17.5 C to 32.5 C.
It will also be noticed that the standard
rate of quiescent periwinkles was always
nearly independent of exposure temperature over the range of tolerance of the organism. The rate of respiration of cell-free
homogenates of the periwinkles is also
shown in Figure 6, and there is also a clear
translation of the point of thermal decline
in relation to environmental temperature
(Newell and Pye, 19716). A similar translation in the thermal tolerance in response
to temperature acclimation has also been
524
RICHARD C. NEWELL
5
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z>o
£.,
10
IS
20
B. HOMOGENATE
T
25
30
35
1
1
I
1
Q
/\
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1
1
0
the thermal tolerance of the system is
raised in response to an increase in environmental temperature. Secondly, the
maximum scope for activity corresponds
with environmental conditions following
acclimation. This in itself may be an important reason why the rate-temperature
relationships of intertidal animals are adjustable, rather than being fixed, and capable of ensuring survival throughout the
environmental temperature range. In this
way, the responses of individual animals
can be delicately adjusted to meet local
conditions as well as allowing wider compensation for latitudinal and seasonal
changes in environmental conditions.
CONCLUSION
EXPOSURE
TEMPERATURE.
C
FIG. 6. Graphs showing the effect of temperature
on the respiration of active and inactive winkles
(Littorina littorea) collected during May, June,
and July 1970. Rate of respiration of cell-free homogenates of the winkles is also shown (after Newell and Pye, 1971b) . Note that translation of the
curves to the right following warm-acclimation is
a common feature of the graphs; also that the active rate is more dependent upon temperature than
is the standard rate of quiescent winkles.
established in this animal and several other intertidal organisms (Vernberg et al.,
1963; Newell et al., 1971a).
In Mytilus ednlis and many other marine invertebrates, this process of adjustment to a new temperature regime normally takes approximately 14 days (Widdows and Bayne, 1972; also Newell and
Pye, 1970&). Figure 7 shows the rate of respiration of two groups of mussels which
had been maintained at 10 C. One group
was placed at 15 C while the other was left
at 10 C and the rate of oxygen consumption was measured over a period of 36
days. The rate of respiration of the mussels
at 15 C was initially high, reflecting the response to acute temperature change, but
after approximately 14 days the rate approached that of the animals at 10 C.
Thereafter, the rates of respiration of the
two groups of mussels were similar.
The effect of such translation of the ratetemperature curves to the right following
warm acclimation is thus twofold. Firstly,
The purpose of this review has been to
demonstrate the complexity and interdependence of many of the factors which influence the respiration of intertidal organisms. Above all, the metabolism of marine
animals is endowed with considerable flexibility between the extremes set by the active and standard rates of respiration. The
process of acclimation primarily involves
an adjustment of physiological processes
such that the maximum scope for activity
coincides with local environmental conditions. The level of respiration in any par-
FIG. 7. Graphs showing the time taken for the
respiration (ml O2/g dry wt/hr) of mussels placed
at 15 C (open circles) to adjust to the same rate as
those at 10 C (closed circles) . Both groups of mussels maintained at 10 C. (Based on Widdows and
Bayne, 1971.)
RESPIRATION OF INTERTIDAL INVERTEBRATES
ticular organism is, however, influenced by
both endogenous and external factors. In.
general, marine organisms display a routine level of activity which is associated
with routine metabolism and is intermediate between the active and standard rates.
Environmental factors normally associated
with the presence of food may induce high
levels of activity in intertidal organisms,
and this is associated with an increase in
the respiration rate from routine levels to
the active rate. The active rate of respiration is markedly temperature dependent in
most instances and may be induced by immersion and disturbance in Littorina (Newell et al., 19716) and bivalves (Morton et
al., 1957) or by the presence of particulate
food in the water (Thompson and Bayne,
1972).
In contrast, situations of environmental
stress such as extremes of temperature or
starvation may reduce the scope for activity and the level of respiration falls from
the routine to the standard rate characteristic of quiescent animals. This may represent an important adaptation to minimize
the use of metabolic reserves during periods of stress and may allow the organism
to increase its activity and metabolic rate
when suitable environmental conditions
prevail. In many intertidal organisms, and
in some subtidal ones, the standard rate has
a low temperature coefficient. It is not
known at present whether this is induced
by tidal-dependent variations in food availability or whether it is a reflection of a
cellular regulatory mechanism which controls the level of substrate available to the
metabolic enzyme systems (Newell and Pye,
197l6,c; Newell, 1973). The resulting virtual thermal independence of the respiration of upper shore animals over the normal environmental temperature range
must, however, further minimize depletion
of the metabolic energy reserves despite the
high environmental temperatures which
often prevail during the intertidal period.
REFERENCES
Ahsanullah, M. 1969. A comparative study of the
effects of desiccation and thermal stress on the
525
intertidal crab Carciuus macnas (L) and the sublittoral crab Porlunas tnarmoreus Leach. Ph.D.
Thesis, University of London.
Ahsanullah, M., and R. C. Newell. 1971. Factors affecting the heart rate of the shore crab Carcinus
maenas (L) . Comp. Biochem. Physiol. 39A:277287.
Ayers, J. C. 1938. Relationship of habitat to oxygen consumption by certain estuarine crabs. Ecology 19:523-527.
Barnes, H., and M. Barnes. 1957. Resistance to
desiccation in intertidal barnacles. Science 126:
358.
Barnes, H., and M. Barnes. 1969. Seasonal changes
in the acutely determined oxygen consumption
and effect of temperature for three common cirripedes, Balanus balanoides (L), B. balanus (L)
and Chthamalus stellatus (Poli). J. Exp. MarBiol. Ecol. 4:35-50.
Barnes, H., M. Barnes, and D. M. Finlayson. 1963.
The metabolism during starvation of Balanus
balanoides. J. Mar. Biol. Ass. U.K. 43:213-233.
Barnes, H., D. M. Finlayson, and J. Piatigorsky.
1963. The effect of desiccation and anaerobic conditions on the behaviour, survival and general
metabolism of three common cirripedes. J. Anim.
Ecol. 32:233-252.
Bayne, B. L., R. J. Thompson, and J. Widdows.
1973. Aspects of temperature acclimation in Mytilus edulis. In W. Wieser [ed.], Effects of temperature on heterothermic organisms. Symposium
1972. Springer-Verlag, Heidelberg. (In press)
Beamish, F. W. H., and P. S. Mookherjii. 1964.
Respiration of fishes with special emphasis on
standard metabolism I. Influence of weight and
temperature on respiration of goldfish Carassius
auratus L. Can. J. Zool. 42:161-175.
Boyden, C. R. 1972. Aerial respiration of the cockle
Cerastoderma edule in relation to temperature.
Comp. Biochem. Physiol. 43A:697-712.
Broekhuysen, C. J. 1940. A preliminary investigation of the importance of desiccation, temperature and salinity as factors controlling the vertical distribution of certain marine gastropods in
False Bay, South Africa. Trans. Roy. Soc. S. Afr.
28:255-292.
Bullock, T. H. 1955. Compensation for temperature in the metabolism and activity of poikilotherms. Biol. Rev. 30:311-342.
Crisp, D. J., and D. A. Ritz. 1967a. Changes in temperature tolerance of Balanus balanoides during
its life-cycle. Helgolaender Wiss. Meeresunters.
15:98-115.
Crisp, D. J., and D. A. Ritz. 19676. Temperature
acclimation in barnacles. J. Exp. Mar. Biol. Ecol.
1:236-256.
Davies, P. S. 1966. Physiological ecology of Patella
I. The effect of body size and temperature on
metabolic rate. J. Mar. Biol. Ass. U.K. 46:647658.
Davies, P. S. 1967. Physiological ecology of Patella
II. Effect of environmental acclimation on the
526
RICHARD C. NEWELL
metabolic rate. J. Mar. Biol. Ass. U.K. 47:61-74.
Davies, P. S. 1969. Physiological ecology of Patella
III. Desiccation effects. J. Mar. Biol. Ass. U.K.
49:291-304.
Dehnel, P. A. 1960. Effect of temperature and salinity on the oxygen consumption of two intertidal crabs. Biol. Bull. (Woods Hole) 118:215249.
Deshpande, R. D. 1957. Ph.D. Thesis, University
of Reading (cited by Fretter and Graham, 1962) .
Dodgson, R. W. 1928. Report on mussel purification. Gt. Brit. Fish. Invest. (Ser. II) 10:1-498.
Edney, E. B. 1960. Terrestrial adaptations, p. 367393. In T. H. Waterman [cd.], The physiology
of Crustacea. Vol. 1. Academic Press, New York.
Edney, E. B., and J. O. Spencer. 1955. Cutaneous
respiration in woodlice. J. Exp. Biol. 32:256-269.
Edwards, G. A., and L. Irving. 1943. The influence
of season and temperature upon the oxygen consumption of the beach flea, Talorchestia megalopthalma. J. Cell. Comp. Physiol. 21:183-189.
Emerson, D., and F. Duerr. 1967. Some physiological effects of starvation in the 'intertidal prosobranch Littorina planaxis (Philippi, 1847). Comp.
Biochem. Physiol. 20:45-53.
Fretter, V., and A. Graham. 1962. British prosobranch molluscs. Ray Society of London.
Fry, F. E. J. 1957. The aquatic respiration of fish,
p. 1-63. In M. E. Brown [ed.], The physiology of fishes. Vol. I. Academic Press, New York.
Fry, F. E. J., and J. S. Hart. 1948. The relation of
temperature to oxygen consumption in the goldfish. Biol. Bull. (Woods Hole) 94:66-77.
Giese, A. 1966. Lipids in the economy of marine invertebrates. Physiol. Rev. 46:244-298.
Gray, I. E. 1953. Comparative study of gill area in
crabs. Anat. Rec. 117:567-568.
Gray, J. 1923. The mechanism of ciliary movement
III. The effect of temperature. Proc. Roy. Soc.
London B 95:6-15.
Hagerman, L. 1970. The oxygen consumption of
Crattgoti vutgaris (Fabricius) (Crustacea, Natantia) in relation to salinity. Ophelia 7:283292.
Halcrow, K., and C. M. Boyd. 1967. The oxygen
consumption and swimming activity of the amphipod Gammarus oceanicus at different temperatures. Comp. Biochem. Physiol. 23:233-242.
Hemmingsen, A. M. 1960. Energy metabolism as related to body size and respiratory surfaces and its
evolution. Rep. Steno. Mem. Hospital 9:7-110.
Hochachka, P. W. 1973. Basic strategies and mechanisms of enzyme adaptation to temperature. In
W. Wieser [ed.], Effects of temperature on heterothermic organisms. Symposium 1972. SpringerVerlag, Heidelberg. (In press)
Hochachka, P. W., and G. N. Somero. 1971. Biochemical adaptation to the environment, p. 99156. In W. S. Hoar and D. J. Randall [ed.], Fish
physiology. Vol. VI. Academic Press, New York.
Jrirgensen, C. B. 1966. The biology of suspension
feeding. Pergamon Press, Oxford.
Kennedy, V. S., and J. A. Mihursky. 1972. Effects of
temperature on the respiratory metabolism of
three Chesapeake Bay bivalves. Chesapeake Sci.
13:1-22.
Kuenzler, E. J. 1961. Structure and energy flow of
a mussel population in a Georgia salt marsh.
Limnol. Oceanogr. 6:191-204.
Lent, C. 1968. Air-gaping by the ribbed mussel
Modiolus demissus (Dillwyn) : effects and adaptive significance. Biol. Bull. (Woods Hole) 134:
60-73.
Mangum, C. P. 1972. Temperature sensitivity of
metabolism in offshore and intertidal onophid
polychaetes. Mar. Biol. 17:108-114.
Mangum, C. P., and C. Sassaman. 1969. Temperature sensitivity o£ active and resting metabolism
in a polychaetous annelid. Comp. Biochem.
Physiol. 30:111-116.
Marsden, I. D., R. C. Newell, and M. Ahsanullah.
1973. The effect of starvation on the metabolism
of the shore crab, Carcinus maenas. Comp. Biochem. Physiol. 45A: 195-213.
Mayer, A. G. 1914. The effects of temperature on
tropical marine animals. Pap. Tortugas Lab.
Carnegie Inst. 6:3-24.
Maynard, D. M. 1960. Circulation and heart function, p. 161-226. In T. H. Waterman [ed.], The
physiology of Crustacea. Vol. 1. Academic Press,
New York.
McFarland, W. N., and P. E. Pickens. 1965. The
effects of season, temperature and salinity on
standard and active oxygen consumption of the
grass shrimp, Palaemonetes vulgaris (Say) . Can.
J. Zool. 43:571-585.
McPherson, B. F. 1968. Feeding and oxygen uptake
of the tropical sea urchin Eucidaris tribuloides
(Lamarck). Biol. Bull. (Woods Hole) 135:308321.
Micallef, H. 1966. The ecology and behaviour of
selected intertidal gastropods. Ph.D. Thesis, University of London.
Micallef, H. 1967. Aerial and aquatic respiration
of certain trochids. Experientia 23:52.
Micallef, H., and W. H. Bannister. 1967. Aerial
and aquatic oxygen consumption of Monodonta
turbinata (Mollusca: Gastropoda) . J. Zool. (London) 151:479-482.
Morton, J. E., A. D. Boney, and E. D. S. Corner.
1957. The adaptations of Lasaea rubra (Montagu) , a small intertidal lamellibranch. J. Mar.
Biol. Ass. U.K. 36:383-405.
Muir, B. S., G. J. Nelson, and K. W. Bridges. 1965.
A method for measuring swimming speed in oxygen consumption studies on the aholehole, Kuhlia sandvicensis. Trans. Amer. Fish. Soc. 90:323327.
Muir, B. S., and A. J. Niimi. 1972. Oxygen consumption of the euryhaline fish aholehole KuhHa sandvicensis) with reference to salinity, swimming and food consumption. J. Fish. Res. Board
Can. 29:67-77.
Neiland, K. A., and B. T. Scheer. 1953. The influence of fasting and of sinus gland removal on
body composition of Hemigrapsus nudus. Phpi-
RESPIRATION OF LNTERTIDAL INVERTEBRATES
ol. Comp. Oceol. 3:321-326.
Newell, R. C. 1966. The effect of temperature on
the metabolism of poikilotherms. Nature (London) 212:426-428.
Newell, R. C. 1969. Effect of fluctuations in temperature on the metabolism of intertidal invertebrates. Amer. Zool. 9:293-307.
Newell, R. C. 1970. Biology of intertidal animals.
Elek Books (Logos Press) , London.
Newell, R. C. 1973. Environmental factors affecting the acclimatory responses of heterotherms. In
W. Wieser [ed.], Effects of temperature on heterothermic organisms. Symposium 1972. SpringerVerlag, Heidelberg. (In press)
Newell, R. C, M. Ahsanullah, and V. I. Pye. 1972.
Aerial and aquatic respiration in the shore crab
Carcinus maenas (L) . Comp. Biochem. Physiol.
43A:239-252.
Newell, R. C, and H. R. Northcroft. 1965. The relationship between cirral activity and oxygen uptake in Balanus balanoides. J. Mar. Biol. Ass.
U.K. 45:387-403.
Newell, R. C, and H. R. Northcroft. 1967. A reinterpretation of the effect of temperature on
the metabolism of certain marine invertebrates.
J. Zool. (London) 151:277-298.
Newell, R. C, and V. I. Pye. 1970a. Seasonal
changes in the effect of temperature on the oxygen consumption of the winkle Littorina littorea
(L) and the mussel Mytilus edulis L. Comp.
Biochem. Physiol. 34:367-383.
Newell, R. C, and V. I. Pye. 1970b. The influence
of thermal acclimation on the relation between
oxygen consumption and temperature in Littorina littorea (L) and Mytilus edulis L. Comp.
Biochem. Physiol. 34:385-397.
Newell, R. C, and V. I. Pye. 1971a. Variations in
the relationship between oxygen consumption,
body size and summated tissue metabolism in the
winkle Littorina littorea. J. Mar. Biol. Ass. U.K.
51:315-338.
Newell, R. C, and V. I. Pye. 19716. Quantitative
aspects of the relationship between metabolism
and temperature in the winkle Littorina littorea
(L) . Comp. Biochem. Physiol. 38B:635-650.
Newell, R. C, and V. I. Pye. 1971c. Temperatureinduced variations in the respiration of mitochondria from the winkle Litlorina littorea (L) .
Comp. Biochem. Physiol. 40B:249-261.
Newell, R. C, V. I. Pye, and M. Ahsanullah. 1971a.
The effect of thermal acclimation on the heat
tolerance of the intertidal prosobranchs Littorina littorea (L) and Monodonta lineata (Da
Costa) . J. Exp. Biol. 54:525-533.
Newell, R. C, V. I. Pye, and M. Ahsanullah. 1971 b.
Factors affecting the feeding rate of the winkle
Littorina littorea. Mar. Biol. 9:138-144.
Patane, L. 1946a. Anaerobiosi in Litlorina neritoides (L). Boll. Soc. Ital. Biol. Sper. 21:928-929.
Patane, L. 19466. Anaerobiosi in Littorina neritoides (L) . Boll. Soc. Ital. Biol. Sper. 22:929-930.
Patane1, L. 1955. Cinesi e teropismi, anidro e anaerobiosi in Littorina neritoides (L). Boll. Accad.
527
Sci. Nat. Gioenia Sper. (IV) 3:65-73.
Pearse, A. S. 1929. Observations on certain littoral
and terrestrial animals at Tortugas, Florida, with
special reference to migrations from marine to
terrestrial habitats. Pap. Tortugas Lab. 26:205223.
Pickens, P. E. 1965. Heart rates of mussels as a
function of latitude, intertidal height and acclimation temperature. Physiol. Zool. 38:390-405.
Precht, H. 1958. Concepts of temperature adaptation of unchanging reaction systems of coldblooded animals, p. 50-78. In C. L. Prosser [ed.],
Physiological adaptation. Amer. Physiol. Soc,
Washington, D. C.
Prosser, C. L. 1955. Physiological variation in animals. Biol. Rev. 30:229-262.
Prosser, C. L. 1958. The nature of physiological
adaptation, p. 167-180. In C. L. Prosser [ed.],
Physiological adaptation. Amer. Physiol. Soc,
Washington, D. C.
Prosser, C. L., and F. A. Brown. 1961. Comparative
animal physiology. 2nd ed. W. B. Saunders Co.,
Philadelphia.
Rajabi, K. G. 1961. Studies on the oxygen consumption in tropical poikilotherms VI. Effect of starvation on the oxygen consumption of the freshwater field crab Paratelphusa sp. Proc. Indian
Acad. Sci. 54:276-280.
Rao, K. P., and T. H. Bullock. 1954. Q,o as a function of size and habitat temperature in poikilotherms. Amer. Nat. 87:33-43.
Read, K. R. H. 1962. Respiration of the bivalved
molluscs Mytilus edulis L. and Brachidontes demissus plicatalus Lamark as a function of size
and temperature. Comp. Biochem. Physiol. 7:89101.
Ritz, D. A., and B. A. Foster. 1968. Comparison of
the temperature responses of barnacles from Britain, South Africa and New Zealand, with special
reference to temperature acclimation in Elminius
modeslus. J. Mar. Biol. Ass. U.K. 48:545-559.
Roberts, J. L. 1957n. Thermal acclimation of metabolism in the crab Pachygrapsus crassipes Randall. I. The influence of body size, starvation and
molting. Physiol. Zool. 30:232-242.
Roberts, J. L. 1957b. Thermal acclimation of metabolism in the crab Pachygrapsus crassipes Randall. II. Mechanisms and the influence of season
and latitude. Physiol. Zool. 30:242-255.
Roy, A. 1963. Etude de l'acclimation thermique
chez la limace Arion circumscriptus. Can. J. Zool.
41:671-698.
Roy, A. 1969. Analyse des facteurs de taux de
metabolisme chez la limace Arion circumscriptus.
Rev. Can. Biol. 28:33-43.
Sandison, E. E. 1966. The oxygen consumption of
some intertidal gastropods in relation to zonation. J. Zool. (London) 149:163-173.
Saunders, R. L. 1963. Respiration in the Atlantic
Cod. J. Fish. Res. Board Can. 20:373-386.
Schick, J. M. 1972. Temperature sensitivity of oxygen consumption of latitudinally separated Urosalpinx cinerea (Prosobranchia: Muricidae)
528
RICHARD C. NEWELL
populations. Mar. Biol. 13:276-283.
Schlieper, C. R. 1952. Uber die Temperatur-stoffwechselrelation einiger eurythermer wassertiere.
Verh. Deut. Zool. Suppl. (16) 5:267-272.
Schlieper, C. R., R. Kowalski, and R. Erman. 1958.
Beitrag zur okologischzellphysiologischen characterisierung des brealen lamellibranchiers Modiolus modiolus L. Kiel. Meeresforsch. 14:3-10.
Scholander, P. F., W. Flagg, V. Walters, and L.
Irving. 1953. Climatic adaptation in arctic and
tropical poikilotherms. Physiol. Zool. 26:67-92.
Somero, G. N. 1969. Enzymic mechanisms of temperature compensation: immediate and evolutionary effects of temperature on enzymes of
aquatic poikilotherms. Amer. Nat. 103:517-529.
Southward, A. J. 1964. The relationship between
temperature and rhythmic cirral activity in some
cirripedia considered in connection with their
geographical distribution. Helgolaender Wiss.
Meeresunters. 10:391-403.
Spoor, W. A. 1946. A quantitative study of the relationship between the activity and oxygen consumption of goldfish, and its application to the
measurement of respiratory metabolism in fishes.
Biol. Bull. (Woods Hole) 91:312-325.
Steeves, H. R. 1963. The effects of starvation on
glycogen and lipid metabolism in the isopod Lirceus brachyurus (Harger) . J. Exp. Zool. 154:2138.
Stickle, W. B., and F. G. Duerr. 1970. The effects of
starvation on the respiration and major nutrient
stores of Thais lamellosa. Comp. Biochem. Physiol. 33:689-695.
Thompson, R. J., and B. L. Bayne. 1972. Active
metabolism associated with feeding in the mussel Mylilus edulis L. J. Exp. Mar. Biol. Ecol. 9:
111-124.
Toulmond, A. 1967a. Etude de la consommation
d'oxygene en function du poids, dans 1'air et dans
l'eau, chez quatre especes du genre Lhtorina
(Gasteropoda, Prosobranchiata) . C. R. Acad. Sci.
Paris 264:636-638.
Toulmond, A. 19676. Consommation d'oxygene,
dans l'air et dans l'eau chez quatre Gasteropodes
du genre Litlorina. J. Physiol. (Paris) 59:303304.
Ulbricht, R. J., and A. W. Prichard. 1972. Effect of
temperature on the metabolic rate of sea urchins.
Biol. Bull. (Woods Hole) 142:178-185.
Vernberg, F. J. 1956. Study of the oxygen consumption of excised tissues of certain marine decapod
Crustacea in relation to habitat. Physiol. Zool.
29:227-234.
Vernberg, F. J. 1959. Studies on the physiological
variation between Uca. II. Oxygen consumption
of whole organisms. Biol. Bull. (Woods Hole)
117:163-184.
Vernberg, F. J., C. Schlieper, and D. E. Schneider.
1963. The influence of temperature and salinity
on ciliary activity of excised gill tissue of molluscs from North Carolina. Comp. Biochem.
Physiol. 8:271-285.
Von Brand, T. 1946. Anaerobiosis in invertebrates.
Biodynamica Monographs. Vol. 4.
Wallace, J. C. 1972. Activity and metabolic rate in
the shore crab, Carcinus maenas (L) . Comp. Biochem. Physiol. 41A:523-533.
Widdows, J. 1972. Thermal acclimation by Mytilus
edulis L. Ph.D. Thesis, University of Leicester.
Zeuthen, E. 1953. Oxygen uptake as related to body
size in organisms. Ann. Rev. Biol. 28:1-12.
Zwaan, A. de, and D. I. Zandee. 1972. Body distribution and seasonal changes in the glycogen content of the common sea mussel Mytilus edulis.
Comp. Biochem. Physiol. 43A:53-58.