Download Calorimetric Studies of Behavior, Metabolism and Energetics of

AMER. ZOOL., 28:161-181 (1988)
Calorimetric Studies of Behavior, Metabolism and Energetics of
Sessile Intertidal Animals1
J. MALCOLM SHICK
Department of Zoology, University of Maine,
Orono, Maine 04469
JOHN WIDDOWS
Institute for Marine Environmental Research, Prospect Place,
Plymouth, England PL1 3DH
ERICH GNAIGER
Institul Zoophysiologie, Universitat Innsbruck,
A-6020 Innsbruck, Austria
SYNOPSIS. Behaviors to conserve water during intertidal exposure at the same time impair
respiratory gas exchange, so that observed responses to emersion may reflect compromises
between these incompatible needs. Behavioral isolation of the tissues from air results in
the complete or partial reliance on anoxic energy metabolism, which is most reliably
measured directly as heat dissipation. Combined direct calorimetry and indirect calorimetry (respirometry) enable the partitioning of total metabolic heat dissipation into its
aerobic and anoxic components, which may vary according to physical and biological
factors. The mussel Mytilus edulis is tolerant of anoxia and saves water and energy during
aerial exposure in its rocky intertidal habitat by closing its shell valves and becoming
largely anoxic. Like most suspension feeders in this habitat, its compensation for reduced
feeding time involves energy conservation; there is little evidence for energy supplementation such as increases in feeding rate or absorption efficiency. Ammonia production
continues during aerial exposure and is involved in acid-base balance in the hemolymph
and mantle cavity fluid. Infaunal cockles (Cardium edule) and mussels (Geukensia demissa)
gape their shell valves, remain largely aerobic and have high rates of heat dissipation
during intertidal exposure, a response which appears related to the lower desiccation
potential and exploitation of richer trophic resources in their soft-sediment habitats. The
variable expansion of the symbiotic sea anemone Anthopleura elegantissima reflects interaction among the responses to desiccation, irradiance and continued photosynthesis by
its zooxanthellae during exposure to air.
"One could safely predict that all physiological processes correspondingly
might be shown to be influenced by the
tide, could we but read delicately enough
the indices."
F F R' k
INTRODUCTION
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The intertidal zone presents a steep gra,•
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mal and osmotic/desiccative, and the
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potentially damaging force or breaking
waves, as well as a decreased time available"
for food capture by sessile suspension feedj - i i-r • u •
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ers. Accordingly,
life in the intertidal zone
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' From the Symposium on Mechanisms of Physioloeical Compensation in Intertidal Animals presented at the
imposes on them not only the challenge of
holding their position, but also a restriction on their energy intake. Moreover,
there is the difficulty of maintaining aerobic respiration in an environment where
most marine invertebrates are morphologically ill-equipped to function and where
behavioral responses to regulate water loss
concomitantly impair gas exchange.
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Despite these rigors, large areas or the
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intertidal zone often are dominated by
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the presence there or unexploited
rood
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resources may have lured motile grazers
such as gastropods into the intertidal zone.
This argument of expansionist exploitatiot
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d o e s
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n l
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sessile
suspension
Annual Meeting of the American Society of Zoolo- feeding epifauna, which probably were
gists, 27-30 December 1985, at Baltimore, Maryland. "bulldozed" Onto hard intertidal Sub161
162
J. M. SHICK ET AL.
strates by bioturbators in soft subtidal sediments (Thayer, 1979), or "chased" there
by predators and competitors: there are
many examples of the lower intertidal limits of sessile fauna being set by the upper
limits of predators or successful competitors {e.g., Connell, 1961; Paine, 1974; Ottaway, 1977).
A critical point is not just that compensations and adaptations relevant to intertidal living exist, but that they can be shown
to vary predictably among individuals and
species occupying different shore heights.
Discerning the interactions among these
morphological, behavioral and physiological/metabolic characters provides a challenge for physiological ecologists and
indeed defines the field of physiological
ecology of intertidal animals. Our approach
to understanding the compensations shown
by sessile molluscs and sea anemones to the
intertidal environment has been to compare the acute and the acclimatized
responses to aerial exposure, and to consider metabolic responses in relation to
other processes such as feeding, digestion,
excretion and growth. An energetic
approach can therefore provide an integration and a means of assessing the overall
performance in terms of the "costs" and
"benefits," and the effectiveness of various
behavioral, physiological and metabolic
responses to environmental change.
anoides and Chthamalus stellatus but lacking
in sublittoral B. crenatus (Barnes et al., 1963).
Moreover, intertidal barnacles become
quiescent during emersion, whereas sublittoral barnacles "struggled erratically and
soon became desiccated" (Barnes and
Barnes, 1957).
Barnacles, like other crustaceans, utilize
the lactate pathway of anoxic energy
metabolism (Barnes et al., 1963). This pathway has a high power output but low energetic efficiency (Gnaiger, 1983a) and often
involves an enhanced anoxic rate of glycolysis (Pasteur effect) compared to the
aerobic rate. Even if there is a reduction
in ATP turnover by quiescent barnacles
during emersion (Barnes et al., 1963), it is
unlikely to be greater in magnitude than
the reduction in ATP yield from lactic acid
production as compared with aerobic respiration, so that a requisite Pasteur effect
to maintain ATP production would more
rapidly deplete glycogen stores. Augenfeld
(1967) observed that high shore species of
barnacles indeed used glycogen more slowly
than did low shore species and had higher
maximum activities of cytochrome oxidase. Thus, the maintenance of aerobic
respiration by intertidal barnacles (Barnes
et al, 1963) appears favored, perhaps to
save energy compared with shifting to lactogenic anoxibiosis.
Unlike barnacles, bivalve molluscs
employ pathways of anoxibiosis which have
BEHAVIORAL AND BIOCHEMICAL
a host of end products other than lactate.
CORRELATES OF INTERTIDAL LIVING
A common feature of these pathways is a
Avoidance of desiccation during inter- greater biochemical efficiency than lactotidal exposure is the foremost constraint genic glycolysis (Gnaiger, 1983a; de Zwaan,
on sessile invertebrates and involves not 1983), which when coupled with a diminonly morphological characters but also ished ATP demand and suppression of the
behaviors which optimize their effective- Pasteur effect, spare glycogen reserves
ness. Behaviors to minimize desiccation when the shell valves close to avoid desicsimultaneously impair respiratory gas cation during exposure to air. That some
exchange, so that overt responses to emer- species do so and others do not seems ultision may reflect compromises between mately related to the desiccation potential
these needs. In Balanus balanoides, the ten- and to the availability of food in their
dency for the barnacles to maintain a respective habitats (see below), as well as
micropylar opening that allowed aerobic to metabolic differences.
respiration to continue during aerial expoAs might be expected in a carnivore,
sure was positively correlated with ambient protein represents a major fuel for aerobic
relative humidity (Grainger and Newell, respiration in the sea anemone Anthopleura
1965). Formation of the micropyle was elegantissima (Zamer and Shick, 1987).
peculiar to intertidal species such as B. bal- Unlike bivalves, sea anemones appear to
CALORIMETRY OF INTERTIDAL ANIMALS
store relatively little glycogen but large
amounts of lipid (Shick, in preparation).
Lipid cannot be a fuel for anoxic energy
metabolism, and the continuation of aerobic respiration by aerially-exposed anemones (Griffiths, 1977; Shick, 1981) may be
related to this fact. Also unlike bivalves,
intertidal sea anemones lack shells and so
are directly exposed to the atmosphere,
which facilitates aerobic respiration but
poses a particular vulnerability to desiccation.
Retention of a large volume of water in
the coelenterons of intertidal actiniid sea
anemones is made possible by their strong
marginal sphincters (Stotz, 1979), coupled
with initial postural adjustments and subsequent quiescence during exposure to air.
That the behavior is associated with regular emersion can be seen by comparing
intertidally acclimatized anemones with
acutely exposed subtidal conspecifics:
whereas the former are quiescent and
maintain a hemispherical shape throughout exposure, the latter are continuously
active and lose much of their coelenteric
fluid (Griffiths, 1977; Shick, 1981). A controlled exudation of coelenteric fluid from
the mouth, as well as evaporation across
the body wall, provides evaporative cooling and allows Actinia equina to survive
higher temperatures in air than in seawater
(Griffiths, 1977).
The attachment of gravel by the verrucae in A. elegantissima establishes a diffusive
boundary layer, reduces desiccation and
enhances survival under extreme conditions (Hart and Crowe, 1977). Again a difference between high and low shore individuals is seen: the former consistently
attach more gravel and shell debris than
do the latter (Dykens and Shick, 1984). The
reflective shell debris may in addition help
to keep body temperature from rising and
so further reduce evaporation. Attached
debris has an additional role, that of "sunscreen," an important consideration in soft
bodied intertidal animals directly exposed
to sunlight. In addition to affording protection from direct photodynamic effects
of ultraviolet radiation on the anemone tissues, the debris may also reduce photosynthesis by the anemone's zooxanthellae in
163
very bright light and thus reduce photosensitized oxidations involving chlorophyll, as indicated by the direct relationship between the amount of gravel attached
by anemones and the chlorophyll content
of their algae (Dykens and Shick, 1984).
Contraction behavior likewise has a role
here: in low to moderate light (and high
relative humidity), the oral disc remains
expanded and allows photosynthesis to
continue, but under very high irradiance,
the marginal sphincter contracts, shading
the algae and reducing photosynthesis
(Shick and Dykens, 1984). Thus the nutritional benefit to the host anemone provided by the zooxanthellae must be behaviorally modulated to reduce potential
detrimental effects inherent in this association. Biochemical and metabolic defenses such as carotenoid pigments, UVabsorbing substances, and enzymes which
detoxify various forms of active oxygen are
attracting increasing attention (see Shick
and Dykens, 1985).
Quiescence during intertidal exposure
not only reduces water loss but also conserves energy, a central tenet of many studies. To some extent this conservation occurs
automatically as suspension feeding activities cease in air, and when avoidance of
desiccation restricts access to atmospheric
oxygen and so reduces the level of aerobic
metabolism, with a diminished energy
demand often being met in part by anoxibiosis. Partial reliance on anoxic energy
metabolism presents a problem to the
experimenter using respirometry because
a greater part of total metabolic rate is
undetected, so that the true energy saving
by quiescence during aerial exposure has
scarcely been investigated. Direct calorimetry, the measurement of metabolic heat
dissipation, is a more general method that
detects all enthalpy changes and so provides the physiological ecologist with the
total heat flux occurring in intertidal animals exposed to air. Whereas intertidallyacclimatized specimens of A. equina remained quiescent and gradually reduced
their rate of heat dissipation during exposure, subtidal individuals acutely exposed
to air became active and maintained a
higher rate of heat dissipation (Fig. 1). The
164
J. M. SHICK ET AL.
Actinia equina
B
A
-1.5
intertidal
12
9
-0.45
-1.0
Subtidal
g
E
-0.30
lntertidaT"~
-1.5
6 6
subtidal
12
1
-0.15 -
I
-1.0
baseline
2
3
4
Time in air (h)
-0.5 K
.- 4
3
4
Time in air (h)
FIG. 1. (A) Continuous recordings of heat dissipation (tQ) in intertidally- and subtidally-acclimatized specimens
of Actinia equina during exposure to air (acute exposure in the latter case). (After Shick, 1981.) (B) Massspecific aerial heat dissipation Qq) and oxygen consumption (rio2) in A. equina. Data are plotted on corresponding
scales using a standard oxycaloric equivalent of 8.000 /rniol O2- h~'/mW. Measured heat dissipation in subtidal
anemones significantly exceeds that calculated from Jio2 from 3.5 hr onward. (From data in Shick, 1981.)
energy conserving effect of quiescence is
highlighted in the power-time (PT) curve
of an intertidally-acclimatized specimen of
M. edulis (Fig. 2D). During the normal 5-hr
period of exposure, the PT curve was
smooth and the rate of heat dissipation low,
but when the mussel was kept in the calorimeter beyond the normal time of reimmersion, it became active and increased its
energy utilization about twofold, the rate
approximating that seen in subtidal individuals. Although such close entrainment
to the tidal cycle may not be the rule in M,
edulis (Gnaiger, 1983c, did not observe this
phenomenon, and Widdows and Shick,
1985, saw it in only one-third of the mussels tested), its occurrence in some individuals at least renders measurable the ofteninvoked but rarely quantified effect of
quiescence on energy expenditure in intertidally acclimatized animals (Newell, 1979).
METABOLISM DURING EXPOSURE TO AIR
Since the seminal studies by Lavoisier
and Laplace two centuries ago, much theoretical and empirical research has confirmed the concordance of heat dissipation
measured directly with that predicted from
the aerobic combustion of organic substrates. This enables the use of indjrect calorimetry (oxygen consumption, A'o2) as a
valid predictor of enthalpy changes asso-
ciated with fully aerobic catabolism through
the use of dissipative (catabolic) oxycaloric
equivalents. During exposure to air, however, bivalve molluscs accumulate end
products of anoxibiosis while simultaneously consuming oxygen (albeit at a lower
rate than occurs during immersion), so that
measurement of oxygen consumption alone
neglects anoxic enthalpy changes and
underestimates total metabolic heat dissipation. Unlike aerobic respiration, the
metabolic changes associated with anoxic
energy metabolism in Mytilus edulis do not
fully account for measured heat dissipation
GQanox). so that there remains a biochemically unexplained "exothermic gap" which
averages 50% of tQanox (Fig. 3). Thus the
sum of enthalpy changes associated with
aerobic and anoxic energy metabolism will
estimate only about 64% of the actual heat
dissipated during an 8 hr exposure to air
in intertidal mussels (Fig. 3).
The advent of calorimeters capable of
measuring the heat fluxes in intertidal
invertebrates enables the quantification of
their total heat dissipation in air and in
seawater (Gnaiger, 19836; Pamatmat,
1983a; Widdows, 1987). The coordinated
measurement of both Aro2 and tQair enables
the partitioning of the latter into its aerobic and anoxic components, for the difference between heat dissipation in air and in
165
CALORIMETRY OF INTERTIDAL ANIMALS
Mytilus edulis
-360
-300
?
.
Most common behavior:
"partial gaper"
®
Natural "gaper"
, (air;
-240
3 "180
"120
-60 " baseline
0
"
'^y-"-""1- ">-
4
Time (h)
Mytilus edulis
-300
•o
-150
.baseline
6
4
Time (h)
i-—t
baseline
4
Time (h)
6
(winter)
LSubtidal
normal relmmersion
Intertidal
-150
4
5
Time (h)
FIG. 2. (A-D) Heat dissipation in individual specimens of Mytilus edulis during exposure to air and to N2 gas.
See text for discussion. (E) Heat dissipation in a specimen of Cardium edule during exposure to air. Sharp
inflection in power-time curve is associated with initiation of air-gaping. (After Widdows and Shick, 1985;
and Snick el al., 1986.)
and in N2 gas is exactly matched by the
caloric equivalent of aerial oxygen consumption (kQox, calculated as No2 times
AvHo2, the oxycaloric equivalent) in M.
edulis (Fig. 4).
Application of direct and indirect calorimetry to intertidally acclimatized individuals of A. elegantissima confirms that they
remain fully aerobic during exposure to
air, despite their lower iVo2 in air than in
water (Shick and Dykens, 1984). The latter
is a consequence of retraction of the tentacles and contraction of the marginal
sphincter, behaviors which not only conserve water but also diminish the respiratory surface area and increase diffusion distances (Shick et al., 1979). Fully aerobic
respiration is also maintained in intertidal
specimens of A. equina, but not in acutelyexposed subtidals, which become active and
maintain a high rate of heat dissipation (Fig.
1A), which is increasingly supported by
anoxic metabolism (Fig. IB) as they lose
their coelenteric fluid and their hydrostatically supported tissues collapse.
The aerobic function of weight-specific
heat dissipation in air, $ air , in M. edulis is
not fixed but may vary according to ration,
acclimatization conditions (subtidal or
intertidal), season, and temperature. The
effect of ration is seen when comparing fed
and fasted individuals (Fig. 5): in the former, the caloric equivalent of oxygen consumption (k<7olt) accounted for 40% of tq3ir,
whereas oxygen consumption was not
detectable in the latter. When the fasted
mussels were again fed at a higher ration
during immersion, they resumed oxygen
consumption when subsequently emersed.
These results suggest that the digestive
process continues during exposure to air,
and either that some aspect of the diges-
166
a>
J. M. SHICK ET AL.
reoxygenation of
hemolymph, tissues,
and mantle fluid
anoxic metabolism during
recovery from prolonged
(24 hr) exposure, involving
accumulation of strombine,
alanine and lactate in
'•.posterior adductor muscle
2a>
Q.0)
3 O)
•"exothermic gap"
conservative, endothermic
processes, including
restoration of high-energy
phosphates and
glyconeogenesis, plus
"endothermic gap"
II
(0 o
.9-o
2
<3
a>
Exposure to air
Recovery in water
Time (hours)
FIG. 3. Schema of heat dissipation and metabolic phenomena in Mytilus edulis during exposure to air and
subsequent recovery in oxygenated seawater during a simulated 12-hr tidal cycle. ,(? is total measured heat
dissipation (heavy continuous line) and iVo, is oxygen uptake (broken line) plotted on the same scale, using
a standard oxycaloric equivalent. ,Q minus the heat equivalent of oxygen consumption in air equals anoxic
heat dissipation, lQmm. JQ_ is that fraction of lQjam that is explained by metabolic changes, the balance representing an unexplained "exothermic gap." Inset: fractions of mQ explained by the enthalpic equivalents of
dissipative ATP turnover associated with the anoxic accumulation of succinate and alanine, and the net
depletion of ATP and phosphoarginine stores. Anoxic metabolism may also occur during recovery from
prolonged exposure or anoxia owing to increased activity of the posterior adductor muscle. See text for
further discussion. (Based on data in de Zwaan et al, 1983; Gnaiger, 1983a; Shick el al., 1983; Shick et al.,
1986; and Gnaiger et al., submitted.)
tion, absorption or assimilation of food
requires O2, or that the large specific
dynamic effect of processing the ingested
ration cannot be met by anoxibiosis alone.
The heat increment associated with feeding and digestion is ~15% of no 2 during
immersion (Widdows and Shick, 1985); this
implies a large energy demand which could
scarcely be met by anoxibiosis, which has
an associated heat dissipation of from 4%
to 13% of the aerobic rate in water in M.
edulis (cf. Famme et al., 1981; Shick et al,
1983; Widdows and Shick, 1985). Since
much of the heat increment of feeding is
due to the mechanical activities of filtration, which ceases during aerial exposure,
the fact that oxygen consumption in air is
one-third of the increment in oxygen
uptake associated with feeding and digestion strongly suggests that this aerobic
component of tQlir supports the additional
metabolic costs of digestion and absorption.
Maintenance of some amount of aerobic
respiration during exposure to air also
depends on the mussels being acclimatized
to such exposure. Subtidally-acclimatized
mussels may not consume oxygen when
acutely emersed (Fig. 5), likely owing to
the tight closure of the shell valves as a
stress response. However, this result varies
seasonally: whereas "winter" mussels
behave as just described, most "summer"
mussels (intertidally and subtidally accli-
167
CALORIMETRY OF INTERTIDAL ANIMALS
-0.25
Mytllus edulis
k«
O)
1
Air
4l
7
i
0L
Air
FIG. 4. Paired measurements of heat dissipation in
four specimens of Mydlus edulis in air and N2 gas at
15°C. The caloric equivalent of oxygen consumption
(k?ox) by mussels in air matches the difference between
,tj,ir and tqama (in N, gas). Combined direct and indirect
calorimetry thus enables the partitioning of iq\ij into
its aerobic and anoxic components. (Mean ± SE.)
(Based on data in Shick et al., 1983.)
Intertidal
(lasted)
Intertidal
(re-fed)
Subtldal
FIG. 5. Effects of feeding, fasting, and resumed feeding on heat dissipation and oxygen consumption in
Mytilus edulis during exposure to air. See text for discussion. (After Widdows and Shick, 1985.)
heat dissipation shown by G. demissa in air
as reflecting the inclusion of an air bubble
matized) do gape in air and have an aerobic during a single gaping event, and gradual
rate of heat dissipation that averages 40% consumption of the O2 in the bubble when
of t<7ail. (Shick et al, 1986). This seasonal the shell valves remained closed. This was
difference may be related to the need for confirmed in a specimen of M. edulis which
evaporative cooling in summer, for the showed a single peak of ,<7air: assuming that
aerobic component of t^air increases with at a respiratory quotient, RQ, of « 1 the
acute exposure temperature (Fig. 6), again gas volume in the bubble remained conlikely owing to an increase in shell valve stant, consumption of all of the O 2 in that
gaping. This behavior is pronounced in bubble was equivalent to 93% of the heat
small individuals of M. edulis (Gnaiger, dissipation integrated above the minimum
1983c), which like small specimens of G. (anoxic) rate (Shick et al., 1986).
demissa, may derive more benefit from
Finally, to emphasize that variations in
evaporative cooling than do large mussels tqair arose from individual differences in air(Lent, 1968).
gaping behavior, mussels forced to gape by
Variability in the PT curves of individual having their shell valves wedged open had
mussels arises from behavioral differences values of tq3ir generally higher than paramong them. Whereas most individuals of tially gaping individuals (cf. Fig. 2A, C), tqair
M. edulis apparently gaped only partially increasing with the volume of enclosed gas
and had a rate of heat dissipation in air two (Shick et al., 1986). Moreover, while the
to three times the anoxic rate in N2 gas PT curves of normal mussels in air are
(Fig. 2A), occasionally the PT curve characteristically rough, likely due to variincreased steeply to a level some four or ation in shell valve activity, those of "forced
five times the initial aerial rate (Fig. 2B), gears" are smooth and lack the peaks and
presumably due to increased shell valve valleys seen in "natural gapers," although
gaping. Volumetric measurement of the gas the maximum rates of heat dissipation are
bubble released by mussels upon reimmer- similar (cf. Fig. 2B, C). Such an effect of
sion revealed a positive relationship continuous oxygen availability was also seen
between bubble size and t^air, with most by Pamatmat (19836) in G. demissa having
individuals having rates of —0.1 to —0.5 their shell valves wedged open.
mW/g dW (Fig. 7). A bubble volume of
There is a direct relationship between
zero corresponded to an anoxic tq of « — 0.1 ^ air and the steady-state rate of heat dissimW/g dW, in agreement with the rates pation in water, tqsl<.zdy, when recovery from
measured in N2 gas (Shick et al., 1986). exposure is complete (Fig. 7, excluding
Pamatmat (1984) interpreted the sharp extreme "gapers"; see below). Although
peaks and subsequent gradual decline in the variability in t^air results from individual
168
J. M. SHICK ET AL.
-320
-
-3.0 -240
-
-2.0 -160 •o-
O
£
6
15
25
-1.0 -
30
Acute exposure temperature (°C)
FIG. 6. Effect of exposure temperature on heat dissipation in Mytilus edulis in air and N2 gas. The
increased aerobic component to heat dissipation (see
Fig. 5) is due to increased air-gaping at the highest
temperature. See text for discussion. (After Widdows,
1987.)
differences in air-gaping behavior, this is
not the case for variable t^steady It appears
that some mussels have a higher energy
demand than others, which is reflected both
in a higher tqsleiAy when immersed and an
increasing aerobic contribution to tqzir
above the anoxic rate when exposed (Fig.
7). When constant difference between tqaaidy
and t<7max (the maximum rate of heat dissipation associated with recovery: see below)
again suggests that in mussels acclimatized
to the same conditions at the same season,
there is a minimum (anoxic) rate of heat
dissipation during aerial exposure in all
individuals which results in a fixed "cost of
recovery" (oct^max - t^steady), and that higher
rates of tqair are supported aerobically.
Differences in air-gaping are also associated with behavioral differences following reimmersion. While "gapers" show very
little shell valve movement during aquatic
recovery, most individuals are more active
(Shick et al., 1986). In both groups there
is a suppression of the activity of the posterior adductor muscle (PAM) during the
first 0.5 hr of reimmersion; together with
the especially wide shell valve gape which
occurs then (Coleman, 1974), this apparently serves to maximize the shell valve
-0.1
anoxic
-0.3
a j r (mW / g)
-0.5
parllally
aerobic
0-*Bubble volume (ml / g)
FIG. 7. Relationship between specific rate of heat
dissipation in air (tq,-,r) and that in oxygenated sea water
during recovery. ,^mlx is the maximum rate of recovery heat dissipation associated with the oxygen debt
payment, and ,^,«ady is the steady-state rate of heat
dissipation when recovery is complete. Volume of air
bubbles enclosed by mussels for which ,q,ir was measured was predicted from measurements of both ,q^r
and bubble volumes released by other mussels upon
reimmersion. See text for discussion. (After Shick et
al, 1986.)
aperture and so minimize resistance to ventilation of the mantle cavity, which promotes the rapid uptake of oxygen and
removal of accumulated ammonia (see
"Reimmersion and Recovery" section).
Subsequent PAM activity may facilitate circulatory perfusion of the tissues, and the
peak in PAM activity coincides with restoration of hemolymph pO2 to its preexposure level (Shick et al., 1986). If, as
in G. demissa and C. edule, maximal air-gaping by M. edulis maintains hemolymph pO2
at nearly the same level as during immersion (Booth and Mangum, 1978; Shick,
unpublished), the near absence of PAM
activity in "gapers" during recovery supports the idea that PAM activity in nongapers is involved with enhanced perfusion
of their tissues by newly reoxygenated
hemolymph. Moreover, most individuals
CALORIMETRY OF INTERTIDAL ANIMALS
of M. edulis show a marked bradycardia
during exposure to air (Coleman and
Trueman, 1971; Shick et al, 1986),
whereas maintenance of higher levels of
cardiac activity by C. edule (Boyden, 1972)
and G. demissa (Booth and Mangum, 1978)
is associated with their pronounced airgaping behavior. Also, the metabolic overshoot associated with repayment of the
oxygen debt is smaller in mussels which
gape during prolonged exposure (Gnaiger
et al., submitted), again suggesting a lower
oxygen demand in "gapers" during early
recovery.
Maximal shell valve gaping and maintenance of high rates of aerial respiration
are the exception in M. edulis, for most
individuals of this species are predominantly anoxic during exposure to air. This
is not the case in C. edule and G. demissa,
which typically gape their shell valves and
maintain high rates of oxygen consumption and heat dissipation (Fig. 2E) that are
from 50% to ~90% of the aquatic rates
(Kuenzler, 1961; Boyden, 1972; Pamatmat, 19836, 1984), with their metabolism
remaining fully aerobic (Widdows and
Shick, 1985). The question arises, what is
the basis for such pronounced behavioral
and concomitant metabolic and energetic
differences between M. edulis on one hand
and C. edule and G. demissa on the other?
Based on experiments by Lent (1968) on
G. demissa, air-gaping does not seem to be
evoked by the need for evaporative cooling, at least in large mussels. Indeed, the
semi-infaunal nature of this species and of
C. edule affords a degree of protection from
elevated air temperatures (Lent, 1968;
McMahon and Wilson, 1981). That airgaping is associated with the successful
occupation of an intertidal habitat is indicated by a close intrageneric comparison:
the predominantly subtidal Cardium
glaucum does not exhibit this behavior and
moreover survives aerial exposure less well
than does C. edule (Boyden, 1972). Since
closing the shell valves, reducing the metabolic rate and relying on efficient anoxibiosis during exposure (and on aerobic
recovery metabolism upon reimmersion:
see below) provide mechanisms to save
169
energy (de Zwaan, 1977; Pamatmat, 1980;
Widdows and Shick, 1985; Gnaiger et al.,
submitted), the question becomes more of
why C. edule and G. demissa do not do this.
Part of the answer may lie in the fact
that these two species seem less well adapted
to survive anoxia than does M. edulis, average anoxic survival at 10°C in C. edule being
4.3 days but 35 days in M. edulis at the same
temperature (Theede et al., 1969). (We note
that 35 days seems a very long survival time
for M. edulis, as Wijsman [1976] found that
mussels were already dying after 7 days of
exposure at 13°C. Also, resistance to anoxia
may not be a constant, for Gnaiger and
Bitterlich [unpublished] observed Cornish
mussels dying after 7 days at 15°C just after
spawning in April, whereas mussels from
the same population survive anoxia for
approximately two weeks in autumn [Shick,
unpublished].) Lent (1968) reports a
median anoxic survival time of 5 days for
G. demissa, apparently at 20-25°C, whereas
this species survives for more than a month
in moist air (Kuenzler, 1961). The shorter
anoxic survival in C. edule may be a consequence of its heavy reliance on lactate
production and maintenance of a relatively
high rate of ATP utilization (Meinardus
and Gade, 1981). The maintenance of a
high rate of energy utilization under anoxia
is also detected calorimetrically, since C.
edule has an anoxic tq that is 42% of the
aerobic ,q (Pamatmat, 1980). Although
anoxic survival times on the order of days
hardly seem relevant to intertidal exposures measured in hours, the differences in
anoxic tolerance may be related to inherent differences in the rate and efficiency of
anoxic energy metabolism and the readiness with which the various bivalves rely
on it (perhaps involving differences in the
speed of transition to the PEPCK route:
Meinardus and Gade, 1981) when exposed
at low tide.
The occupation of an exposed rocky
intertidal habitat by epifaunal Mytilus edulis
exposes it not only to desiccating conditions but also to a low availability of food,
both of which factors select for behaviors
such as shell valve closure to conserve water
and energy. The closely controlled air gap-
170
J. M. SHICK ET AL.
ing behavior in this species may at times
promote evaporative cooling, but also
seems to regulate a variable aerobic component of total energy metabolism to support the costs of digestion and absorption
when food is present in the digestive system. Occupation of trophically rich mudflats and salt marshes by Cardium edule and
Geukensia demissa places them in a position
to exploit abundant food, especially as
feeding may continue when they filter tidal
runoff or interstitial water after the tide
has receded. Moreover, the costs of continued digestive processes during intertidal
exposure may necessitate a major reliance
on aerobic respiration, as argued for M.
edulis. In short, the physical nature of the
substrates where they occur is linked to
trophic richness, and may allow C. edule
and G. demissa to exploit this richness without the constraint of behaviors geared to
avoiding desiccation. The interplay of
behaviors to conserve water while at the
same time enhancing energy acquisition is
particularly apparent in the symbiotic sea
anemone Anthopleura elegantissima: retraction of the tentacles and assumption of a
hemispherical shape saves both water and
energy during emersion, but the variable
exposure of the oral disc depending on
ambient humidity and irradiance allows
photosynthesis and partial autotrophy to
continue. Actinia equina lacks algal symbionts and remains fully contracted during
exposure, there being no energetic advantage to partial expansion.
REIMMERSION AND RECOVERY
A major feature of recovery from aerial
exposure shown by nearly all intertidal animals is the overshoot in oxygen uptake,
known as the oxygen debt payment, immediately following reimmersion in oxygenated seawater. This occurs during recovery
from both environmental hypoxia and
physiological hypoxia, such as that caused
by intense muscular activity. Respirometric studies have shown that the size of the
oxygen debt payment by intertidal animals
depends on body size, the duration of aerial
exposure, behavior, ration and temperature. The relationship between the size of
the oxygen debt payment and body mass
in M. edulis is described by a mass exponent
("b") of 0.74, identical to the b value for
the aquatic rate of oxygen uptake (Widdows and Salkeld, unpublished). In species
and individuals that remain closed during
aerial exposure, part of the total oxygen
debt payment is the physical reoxygenation of body water, such as mantle cavity
fluid in bivalves, and intra- and extracellular fluids (Fig. 3). The reoxygenation
component forms approximately 15% of
the total oxygen debt payment in M. edulis
(Widdows and Shick, 1985; Gnaiger et al.,
submitted; Shick et al., 1986), the remainder representing the metabolic oxygen debt
payment.
Various authors have shown that the size
of the oxygen debt payment increases with
the duration of aerial exposure, at least
over a period of 12-16 hr for mussels (Fig.
8). For the sea anemone Bunodosoma cavernata, Ellington (1982) has shown that the
magnitude of the oxygen debt payment
increases with the duration of exposure to
anoxia in seawater, whereas intertidally
acclimatized individuals of Anthopleura elegantissima remain fully aerobic during aerial
exposure and show no oxygen debt payment (Shick, 1981). However, bivalves such
as G. demissa and C. edule, which gape and
consume large amounts of oxygen during
aerial exposure, also show a distinct overshoot in oxygen uptake upon reimmersion
(Widdows et al., 1979; Widdows and Shick,
1985).
Ration not only affects the steady rate of
aquatic oxygen consumption by M. edulis
but also the maximum rate after reimmersion as well as the size of the metabolic
oxygen debt payment in a similar proportional manner (Widdows and Shick, 1985).
Widdows et al. (1979) have demonstrated
an effect of air temperature on the size of
the oxygen debt payment, with a marked
increase in both M. edulis and C. edule when
exposed to a 10°C increase in air temperature, probably as a consequence of the
thermal dependence shown in the aerial
rate of heat dissipation (Fig. 6).
Although the oxygen debt payment associated with recovery from environmental
anoxia and hypoxia has been described in
many studies and reviewed by Herreid
CALORIMETRY OF INTERTIDAL ANIMALS
171
32
24
•
0
O
A
A
Bayne et a i d 976) -littoral M. callfornianus
De Vooys & De Zwaan(1978) -sublittoral M. edulis
De Vooys a De ZwaarK1978) -littoral M. edulis
Widdows et al(1979) -littoral M. edulis
Widdows & Shick(1985) -littoral M. edulis
16
o
E
s
n
o>
•a
0
Amount of O 2 required to resaturate mantle cavity water
& body fluids
36
'
'
48
12
24
Hours of exposure to air
FIG. 8. Relationship between the duration of aerial exposure and the size of the oxygen debt payment by
Mytilus edulis and M. californianus.
(1980), an adequate metabolic interpretation cannot be provided without a combination of direct calorimetry and indirect
calorimetry, such as respirometric and biochemical measurements (Shick and Widdows, 1981; Shick et al., 1983; Gnaiger et
al., submitted). The marked reduction in
the anoxic rate of heat dissipation to
approximately 4-7% of the aquatic aerobic
rate, and the concomitant suppression of
the Pasteur effect noted by de Zwaan and
Wijsman (1976), represent aspects of the
"energy saving" mechanism during aerial
exposure or anoxia. But any evaluation of
"energy saving" must take into account the
"cost of recovery" (Shick and Widdows,
1981; Widdows and Shick, 1985). Furthermore, any energy saving associated
with reduced heat dissipation during aerial
exposure would be in vain if accumulated
glycolytic end products were then excreted
or completely burned during recovery and
payment of the oxygen debt (Gnaiger et al.,
submitted).
The use of simultaneous, or coordinated
non-simultaneous, direct and indirect calorimetry under conditions such as aerial
exposure, anoxia and recovery, not only
provides a direct measurement of total
metabolic heat dissipation but also quantifies the heat equivalent of oxygen uptake
and thus indicates the nature of the metabolic processes, such as the degree of
anoxibiosis or conservative anabolism. The
heat or oxycaloric equivalent of aerobic
catabolism ranges from —440 to —480 k j /
mol O2 (Gnaiger, 1983a), and a dissipative
oxycaloric equivalent of —450 kj/mol O 2
is commonly used to calculate metabolic
heat loss in respiratory studies and the construction of energy budgets. However,
calorimetric studies have shown that there
are marked changes in the heat equivalent
of oxygen uptake both during aerial exposure (see previous section) and aquatic
recovery (Gnaiger et al., submitted).
Figure 9 demonstrates that during aerial
exposure the empirically derived heat
equivalent exceeds the theoretical range,
thus indicating anoxibiosis. The higher the
172
J. M. SHICK ET AL.
-600
I -500
Theoretical range of
oxycaloric equivalents for
totally aerobic metabolism
CD
-400
o
o
'c
-300
CO
>
tT
01
-200
CO
<u
I
-100
8
12
16
20
Hours (Recovery)
FIG. 9. Effect of the duration of anoxia on the heat equivalent of oxygen uptake by Mytilus edulis during
recovery in air-saturated seawater. See text for discussion. These long-term experiments were enabled by the
development at IMER, Plymouth, of a perfusion system for an LKB microcalorimeter which allows simultaneous measurement of heat dissipation and oxygen consumption by animals of up to 1 g dry mass, using a
flow rate of up to 120 ml/hr. (Gnaiger, 1983c; Widdows and Salkeld, unpublished).
experimental heat equivalent of O2 uptake,
the greater the reliance on anoxic metabolism. For example, intertidal individuals
of M. edulis have a heat equivalent of
-1,250 kj/mol O 2 (Widdows and Shick,
1985). The value of - 5 5 0 kj/mol O2 for
subtidal Actinia equina suggests a smaller
anoxic component (Fig. 1) , and —455 k j /
mol O 2 for intertidal C. edule indicates fully
aerobic metabolism (Widdows and Shick,
1985).
Conversely, if the total heat equivalent
of oxygen uptake falls below the theoretical range, such as during recovery, then
net biosynthesis giving rise to endothermic
anabolic heat changes is suggested. The
extent to which the heat equivalent falls
below —440 kj/mol O 2 increases with the
duration of aerial exposure (Fig. 9). Consequently, the application of a standard
oxycaloric equivalent of —450 kj/mol to
convert the metabolic oxygen debt payment to metabolic heat loss will overestimate the energy expenditure during recovery perhaps by 20% during the initial hour
of recovery (-360 kj/mol O2) and by 12%
later in recovery ( — 400 kj/mol O 2 ),
although this may be complicated by anoxic
energy changes then (Gnaiger et al., submitted).
Recently, we have used a combined direct
and indirect calorimetric approach to
advance the interpretation of metabolic
events occurring during the anoxic—aerobic transition (recovery) in M. edulis
(Gnaiger et al., submitted). Although the
results are based on extended (24 hr)
periods of aerial exposure, because the
effects are more marked and readily
detectable, more recent evidence confirms
CALORIMETRY OF INTERTIDAL ANIMALS
that the responses to shorter and more ecologically relevant periods of aerial exposure are of a similar nature, varying only
in degree (Shick et al, 1986).
To enable direct comparison of heat dissipation and oxygen uptake during recovery, they are plotted on corresponding
scales based on the catabolic oxycaloric
equivalent (Fig. 3). Recovery from 24 hr
of aerial exposure can be divided into two
distinct phases: early recovery in the first
hour, characterized by the maximum rate
and minimum caloric equivalent of oxygen
uptake, and late recovery (1-3 hr), featuring a higher caloric quotient and a rate
gradually declining toward the steady state.
The functional complexities of recovery
metabolism are most clearly seen in an
analysis of net recovery processes, removing the variability of aerobic steady-state
rates.
After correction for the reoxygenation
of mantle cavity water and body fluids, the
caloric quotient of net recovery oxygen
consumption is — 252 kj/mol O2 (total
caloric quotient is —366 kj/mol O2) during early recovery, indicating conservation
of heat in endothermic processes. After
accounting for conservation of heat in the
ergobolic debt payment {i.e., the restoration of high-energy phosphates with catabolic-ergobolic coupled metabolism: see
Gnaiger, 1983a), the caloric quotient of
residual net recovery oxygen consumption
of —260 kj/mol O2 still indicates highly
conservative processes. These can also
explain previous discrepancies in biochemical studies by de Vooys and de Zwaan
(1978) and Widdows et al. (1979), in which
the size of the oxygen debt payment was
less than the amount of O2 required for
the complete oxidation of accumulated end
products such as succinate, alanine and
propionate. There is no evidence of excretion of succinate or alanine, but some propionate may be excreted or reabsorbed by
mussels during recovery (Zurburg et al.,
1982). On the basis of metabolic acid quotients (molar AQ, analogous to RQ), and
stoichiometric and thermodynamic considerations, there is a postulated mechanism
whereby six times more succinate can be
discharged in catabolic-anabolic coupled
173
glyconeogenesis and in partial oxidation of
succinate to malate and aspartate, as compared with the complete oxidation of succinate (Gnaiger et al., submitted). Furthermore, the theoretical conservative caloric
equivalent of oxygen consumption in fully
catabolic-anabolic coupled recovery is as
low as —200 kj/mol O 2 on the basis of
succinate.
Although most of the observed changes
in biochemistry, heat dissipation and oxygen uptake can be explained, the recovery
oxygen consumption is higher than the
oxygen debt expected on the biochemical
basis of a highly conservative AQ. The
excess conservative respiration during early
recovery represents an "endothermic gap"
(Fig. 3), the size of which is in close agreement with the size of the "exothermic gap,"
the excess heat observed during anoxia,
which suggests some compensatory reversal during recovery of the biochemically
unexplained exothermic gap under anoxia
(Gnaiger et al., submitted). Here again are
important similarities between environmental anoxia and recovery in mussels and
physiological anoxia and recovery in vertebrate muscles (cf. Curtin and Woledge,
1978; Gnaiger, 1983a).
In contrast to early recovery, during the
late recovery period between 1 and 3 hr,
there is a transient increase of total heat
dissipation above the standard caloric
equivalent of oxygen consumption (Fig. 3).
This results in a high caloric quotient of
— 584 kj/mol O2 of net recovery oxygen
consumption (total caloric quotient is —503
kj/mol O2). Since the timing of this high
oxycaloric quotient precisely matches the
time course of strombine, alanine and lactate accumulation in the posterior adductor muscle ofMytilus edulis (de Zwaan et al,
1983), this high oxycaloric quotient suggests the occurrence of anoxic metabolism
during late recovery, but the timing does
not support the contention that anoxibiosis
is invoked to compensate for a limited
aerobic capacity in the oxygen debt payment (Fig. 3). The accumulation of strombine and lactate in the posterior adductor
muscle correlates with the frequency of
shell valve adductions which peak at ca. 12 hr after reimmersion (Shick et al., 1986).
174
J. M. SHICK ET AL.
Reimmersion
Exposure to air
\\\\\\\\\\\\\\\\\\\\\\\\\\\\\\\\\v
12
18
30
Hours
FIG. 10. Ammonia accumulation in hemolymph and mantle cavity water of Mytilus edulis during 24 hr of
aerial exposure, and ammonia excretion rate before and after exposure. (Mean ± SE: n = 10.) (Widdows,
unpublished.)
Hence anoxic energy metabolism is
required to meet the increased energy
demands associated with muscular activity.
Although the role of this muscular activity
is unclear, it may be related to enhanced
perfusion of the tissues with reoxygenated
hemolymph, as discussed in the previous
section. This anoxic component is not
always apparent during recovery because
ongoing endothermic reactions and individual variability in non-simultaneous mea-
surement of heat dissipation and oxygen
uptake may mask the exothermic heat
changes.
In contrast to bivalves, Ellington (1982)
found that the overshoot in oxygen uptake
by the anemone Bunodosoma cavernata,
although not corrected for reoxygenation
of body fluids following anoxia, appears to
exceed that required to oxidize the accumulated end products. This difference is
probably related to the nature of the end
175
CALORIMETRY OF INTERTIDAL ANIMALS
T A B L E 1.
Effect of aerial exposure on the rale of ammonia excretion by bivalves.
Species
Mytilus californianus
Mytilus edulis
Cardium edule
Rate of ammonia accumulation in hemolymph and Rate of ammonia excremantle cavity water
tion (subtidal aauatic
during aerial exposure
steady rate;
/imoles N H 4 * g ' d W h r ' *imoles N H / g " 1 d W-hr'
0.07
0.11
0.213*
2.14
1.04
0.425
Aerial rate as %
of aquatic rate
3-6%
11%
50%
Reference
Bayne et al. (1976)
Widdows (unpublished)
Widdows and Shick (1985)
* Based on NH4+ released upon reimmersion.
protein or free amino acids cannot be ruled
out. It may also be that sea anemones rely
heavily on protein as a substrate for anoxic
energy metabolism, just as they do in aeroAMMONIA PRODUCTION
bic respiration (Zamer and Shick, 1987).
Ammonia is another metabolic end The former is indicated in studies by
product which accumulates at a steady rate Ellington (1977, 1980, 1982) and Navarro
within the hemolymph and mantle cavity and Ortega (1984), where predominantly
fluid of mussels during aerial exposure nitrogenous end products such as alanine
(Bayne et al, 1976; de Zwaan et al, 1983; and glutamate accumulate. In addition,
Fig. 10). However, de Zwaan et al. (1982, Ellington (1982) has shown that the
1983) have shown that relatively little increase in ammonia excretion by B. cavammonia accumulates in the tissues of M. ernata during recovery from anoxia agrees
edulis during 24 hr of exposure to air. closely with that predicted from the decline
Ammonia accumulates in both the hemo- in alanine concentration in the tissues.
lymph and mantle cavity fluid at a steady Unfortunately, the accumulation of
rate of «0.1 ^mol-hr~'-g~' mussel dry ammonia during anoxia or aerial exposure
mass, reaching concentrations of 200 nM has not been tested in sea anemones.
(Fig. 10) to > 400 MM(de Zwaan <?/«/., 1983).
If ammonia is excreted from the cells as
The rate of ammonia excretion into the gas, it may play a role in acid-base balance
two compartments (Table 1) is approxi- in the extracellular fluids of bivalves durmately 3 to 30% of the normoxic aquatic ing periods of hypoxia (perhaps reducing
rate of ammonia excretion by M. edulis, the amount of shell decalcification that
and therefore shows a proportional change occurs then), by the protonation of ammosimilar to that observed for total energy nia to the ammonium ion. Booth et al.
metabolism. This relationship is also dem- (1984) showed that this may account for as
onstrated in the air-gaping C. edule, which much as 30% of the combined Ca + + and
has aerial rates of ammonia production and NH4+ buffering in the hemolymph of M.
energy metabolism that are ~50% of the edulis during 8 hr of exposure to air,
aquatic rates (Widdows and Shick, 1985). although increases in Ca + + and NH4+
Although it generally has been assumed accounted for only 50% of an observed base
that the ammonia produced in bivalves excess.
during exposure to air is derived from
Upon reimmersion, typically there is an
aerobic metabolism, Bitterlich and Gnaiger immediate release of ammonia by bivalves,
(unpublished data) have shown that ammo- with the exchange of mantle cavity water,
nia continues to accumulate in M. edulis and this is accompanied by a rapid loss of
during 5 days of anoxia. Some of this ammonia from the hemolymph during the
ammonia may be produced by deamination first hour (Fig. 10). Bayne et al. (1976) and
of AMP, as the concentration of total ade- de Vooys and de Zwaan (1978) found that
nylates in some tissues of M. edulis declines the amount of ammonia released by M. calslightly during prolonged anoxia (Wijs- ifornianus and M. edulis is proportional to
man, 1976), although anoxic catabolism of the duration of aerial exposure, which is
products, because anoxia does not produce
significant changes in succinate, rather,
mainly alanine and glutamate accumulate.
176
J. M. SHICK ET AL.
in agreement with a steady rate of ammonia accumulation during exposure (Fig. 10).
During the spring and summer, a time
of abundant food and growth, aerial exposure results in a distinct overshoot in
ammonia excretion byM. rfufo upon reimmersion, with ammonia accumulated in the
mantle cavity and hemolymph accounting
for 35 to 75% of ammonia excreted during
the first hour. Conversely, during the
autumn and winter, there is evidence of
reduced ammonia excretion with no overshoot upon reimmersion. Specimens of M.
edulis, both intertidally acclimatized and
acutely exposed to 5 hr in air and 7 hr in
water, reduce their rates of ammonia
excretion over this 12 hr period to 14%
and 65%, respectively, of the aquatic rates
(Widdows and Shick, 1985). This suggests
nitrogen conservation at this time of year
(de Zwaan et al., 1983; Hawkins, 1985).
This is in contrast to air-gaping bivalves
such as C. edule (Widdows and Shick, 1985)
and G. demissa (Jordan and Valiela, 1982),
which maintain a daily rate of ammonia
excretion independent of aerial exposure
time. Furthermore, C. edule shows a distinct overshoot in ammonia excretion following reimmersion which reflects a flushing out of ammonia accumulated in the
hemolymph and mantle cavity fluid during
exposure.
EFFECT OF TIDAL LEVEL ON THE
ENERGETICS OF INTERTIDAL ANIMALS
An energetic approach, based on the
integration of rates of feeding, food
absorption, total energy metabolism,
excretion, growth and reproduction, provides a useful means of assessing the overall
performance of an animal. Individual components of the energy budget should not
be considered as isolated processes. The
benefits derived from energy conservation
during intertidal exposure have their costs
in terms of aquatic recovery and the
restrictions placed on feeding, digestion
and biosynthesis, while any benefits derived
from enhanced feeding activity have their
associated metabolic costs; together they
may be regulated to maximize or optimize
the net energy gain.
The net energy available for growth and
reproduction, the "scope for growth," is
the difference between energy acquired
from food and the energy expended in
metabolism and excretion. The relative
contributions made to the intertidal growth
performance of bivalves by "energy-conserving" and "energy-supplementing"
capacity adaptations have been considered
by Gillmor (1982).
Energy conservation during aerial exposure and anoxia has been suggested by
many authors (e.g., de Zwaan and Wijsman,
1976;Bayne?/a/., 1976; Pamatmat, 1979;
Widdows et al., 1979) but the overall heat
loss by intertidal bivalves during exposure
and recovery has only recently been quantified (Widdows and Shick, 1985; Gnaiger
et al., submitted; Shick et al., 1986). Mytilus edulis, which gapes only slightly during
aerial exposure, reduces its daily rate of
heat dissipation by 34% when acclimatized
to a 42% air exposure regime in a tidal
simulator, whereas subtidally acclimatized
individuals acutely exposed to air reduce
daily heat dissipation by only 17% compared to the steady state subtidal rate (Widdows and Shick, 1985). In contrast, C. edule,
which typically gapes during exposure,
reduces its daily energy expenditure by 29%
when intertidally acclimatized and by only
9% when acutely exposed to air.
Energy acquisition may be enhanced by
increasing feeding and ingestion during
immersion, and continuing digestion and
absorption during emersion when feeding
ceases. Increases in feeding rate, albeit
transitory, in response to regular aerial
exposure have been reported in three suspension feeders- the bivalve Lasaea rubra
(Morton etal., 1957), the barnacle Balanus
balanoides (Ritz and Crisp, 1970), and the
sea anemone Anthopleura elegantissima
(Zamer, 1986), and in the grazing gastropods Littorina littorea (Newell et al., 1971)
and Melagraphia aethiops (Zeldis and Boyden, 1982).
Only A. elegantissima has been studied
with respect to multiple components of the
energy budget. Anemones aerially exposed
for 75% of the time exhibited both energy
conserving and energy supplementing
adaptations compared with subtidally acclimatized conspecifics (Table 2). Scope for
177
CALORIMETRY OF INTERTIDAL ANIMALS
TABLE 2. Energy budgets ©/"Anthopleura elegantissima/rom high and low shore levels.*
Tidal height
High
Low
Dry
weight (g)
Daily immersion Daily ration
(hr)
(mgday 1 )
6
22
6.35
7.24
Ingestion
rate
(kj-day-)
Paniculate
absorbed
energy
(kj-day-')
CZAR*
(kj-day-')
0.158
0.180
0.151
0.166
0.031
0.112
Energy
Total assimi- respired and
lated energy
excreted
(kJ-day-'J
(kjday-)
0.182
0.278
0.075
0.140
SFG*
(kjday-)
0.107
0.138
• From Zamer and Shick, 1987.
b
CZAR = contribution of zooxanthellae to animal's respiratory requirements.
c
SFG = scope for growth.
growth was disproportionately large in the
high shore anemones relative to their long
exposure as a result of lower metabolic costs
during aerial exposure (Shick, 1981;
Dykens and Shick, 1984) combined with
increased rates of prey capture during
immersion and higher absorption efficiencies (Zamer, 1986). There were no differences in their feeding surface area, but high
shore anemones appeared more receptive
to prey.
There is no evidence of major compensatory increases in the overall feeding rates
or absorption efficiencies of most intertidal
bivalves, including M. edulis (Jergensen,
1960; Widdows and Shick, 1985), Choromytilus meridionalis (Griffiths, 1981; Griffiths and Buffenstein, 1981), G. demissa
(Jordan and Valiela, 1982) and C. edule
(Widdows and Shick, 1985), with increasing height on the shore. However, intertidally acclimatized bivalves appear to pump
more or less continuously when immersed
compared with a more variable and intermittent pumping by subtidal bivalves
(Brand and Taylor, 1974; Widdows and
Shick, 1985). Further intraspecific compensations for a reduction in feeding time
include a more rapid resumption in feeding activity by intertidally acclimatized
individuals compared with subtidal specimens of C. edule, which results in a more
rapid establishment of a positive scope for
growth (Widdows and Shick, 1985). In
addition, there are interspecific differences, with higher shore species such as L.
rubra (Morton et al., 1957) and M. edulis
resuming feeding more rapidly than lower
shore species such as C. edule (Widdows and
Shick, 1985).
Part of any energy supplementation may
also arise from a tidally synchronized diges-
tive rhythm and from adaptations that
maintain some digestive and absorptive
activity during aerial exposure, thus
enhancing daily food absorption (L. rubra,
Morton, 1956;M. edulis, Langton and Gabbott, 1974; Langton, 1975, 1977; Robinson et al., 1981; M. californianus, Thompson et al., 1978; Crassostrea gigas, Morton,
1977). However, any extra food absorption is only apparent as a transient response
immediately after reimmersion (Widdows,
unpublished; Bayne et al., 1988), because
Griffiths and Buffenstein (1981), Jordan
and Valiela (1982) and Widdows and Shick
(1985) found no evidence of a marked
change in overall absorption efficiency in
intertidally acclimatized cockles and mussels, compared with low shore or sublittoral individuals.
The net effects of energy conservation
and energy supplementation on the energetics of M. edulis and C. edule are summarized in Table 3. Although aerial exposure resulted in a reduction in scope for
TABLE 3. Effect of 10 hrday' aerial exposure (i.e., 427c)
on the daily scope for growth and net growth efficiency (K^j
ofMytilus edulis and Cardium edule.*
Scope for erowlh
Species/condition
Mytilus edulis (1 g)
Intertidal
Subtidal
Acute air exposure
Intermittently fed
Continuously fed
Cardium edule (0.3 g)
Intertidal
Subtidal
Acute air exposure
Intermittently fed
Continuously fed
* Widdows and Shick, 1985.
(Jday-)
K,
+ 65
0.50
+45
+ 36
+ 122
0.36
0.26
0.55
+ 13
0.19
-14
-8
+64
—
—
0.46
178
J. M. SHICK ET AL.
growth compared to the continuously fed
subtidal individuals, the intertidally acclimatized mussels had a higher scope for
growth relative to the subtidal individuals
acutely exposed, which had a higher value
than the subtidal, intermittently fed individuals given the same daily ration as intertidals and acutely exposed subtidals. However, the net growth efficiency (K2) of the
intertidal group was similar to the subtidal
continuously fed group. In comparison,
aerial exposure had a more adverse effect
on C. edule, both in terms of scope for
growth and growth efficiency, indicating
little compensation in terms of either
energy conservation or supplementation on
the relatively low ration provided in that
study.
Aerial exposure affects not only the total
energy available for production, but also
the partitioning between somatic growth
and reproduction. Griffiths (1981) has
demonstrated that high shore C. meridionalis reduces the energy allocation to
somatic growth and directs a greater proportion of the available energy to reproduction, thus maintaining a high reproductive output. A similar phenomenon was
seen in M. edulis (Rodhouse et al., 1984).
The high growth rates in high shore specimens of Anthopleura elegantissima (Zamer,
1986) may be directed toward the rapid
achievement of the minimum size necessary for reproduction in this anemone, in
spite of the reduced time available for feeding, and Sebens (1981) showed that high
shore individuals had the same or greater
gonad production than low shore anemones.
Finally, the effect of aerial exposure on
the growth rate of immature individuals of
several intertidal bivalves species was
assessed by Gillmor (1982) in both laboratory and field studies. In the case of lower
shore species such as Modiolus modiolus and
Ostrea edulis, the observed growth was less
than the hypothetical growth strictly determined by the time available for feeding,
due to the lack of energy conservation or
supplementation, and the predicted zero
growth level was at 24% and 52% air exposure, respectively. The growth rates of M.
edulis and C. virginica both were slightly
above the hypothetical growth curves due
to energy conservation and some minor
energy supplementation. The predicted
upper limit of growth was at 80% to 85%
aerial exposure.
In the ribbed mussel, G. demissa, the
growth rate was substantially higher in the
intertidal zone compared to the subtidal,
but the upper limit to growth could not be
established from the data. Lent (1969) and
Jordan and Valiela (1982) did not record
any energy conservation or supplementation by high shore specimens. But continued growth of G. demissa in the high intertidal zone may be related to the gill
structure in this species, which allows the
efficient retention of bacteria-sized particles, thus increasing food availability in a
rich salt marsh habitat (Wright et al., 1982).
Further integrated studies on this species
are clearly needed.
Not surprisingly, these findings suggest
that the observed growth rates of each
species in relation to aerial exposure are
in good agreement with the shore position
they occupy in nature, and differences in
growth can largely be explained in terms
of behavioral, physiological and biochemical factors. However, the upper limit of
growth and survival and the tolerance of
aerial exposure are modified by environmental factors, particularly food resources
and air temperatures. Productive soft-sediment habitats, such as marshes, increase
food availability for mussels such as G.
demissa, thereby enabling them to exploit
higher shore levels despite shorter feeding
periods. The adoption of an infaunal habit
in muddy substrata by G. demissa and C.
edule also ameliorate the effects of elevated
air temperatures and minimize desiccation. Conversely, M. edulis is able to exist
in a hard-substrate intertidal habitat, where
it is more directly exposed to air and where
food resources are usually more limited,
because of its greater tolerance of anoxia
and its behavioral and physiological adaptations that conserve both energy and
water.
ACKNOWLEDGMENTS
Much of the research reviewed here was
supported by U.S. National Science Foun-
CALORIMETRY OF INTERTIDAL ANIMALS
dation grants PCM79-11027 (Regulatory
Biology) and SPI80-13119 (Science Faculty Professional Development) to J.M.S.
E.G. was supported by the Fonds zur Forderung der wissenschaftlichen Forschung
in Osterreich, project J0011, and by a British Council Scholarship. Collaboration
among ourselves and B. L. Bayne and A.
de Zwaan was facilitated by NATO
research grant 27181. We also thank G.
Bitterlich for unpublished data.
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