A M . ZOOLOGIST, 11:571-576 (1971).
Pressure Effects on the Respiration of Vertically Migrating
Decapod Crustacea
JOHN M. TEAL
Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543
SYNOPSIS. The respiration o£ five species oC North Atlantic decapods was measured
under conditions of pressure and temperature which allow calculation of the metabolism of these animals in the oceans. The species were: Systellaspis debilis, Acanthephyra purpurea, Oplophorus sphiosus, Parapandalus richardi, and Sergestes crassus.
Results indicate a tendency for metabolism to remain relatively constant with depth,
the decrease due to lower temperature offset by an increase due to rising pressure.
This contrasts with previous work with epipelagic euphausids which tended to have
greatly reduced metabolism with increasing depth. Perhaps the metabolic rate of the
decapods must remain high enough for them to remain effective predators throughout
their depth range, by day as well as night.
Vertically migrating animals in the scattering layers of the oceans experience daily
changes in both pressure and temperature. Surface dwellers are subject to temperature changes but not to pressure
changes of any significance as far as direct
effects upon their metabolism are concerned. Deep-sea animals are subject to
high pressures and low temperatures but
little in the way of changes in either
parameter. But animals migrating over
vertical distances of as much as 1000 meters may spend the night at temperatures of
20°C and pressures of a few atmospheres
and the day at 100 atmospheres and 4 to
7°C.
Vertically migrating animals have had
adequate time to evolve adaptions to these
changes and, even if they follow the usual
pattern of showing a greater pressure
effect at high temperatures than at low,
they could theoretically show a decrease,
an increase, or no change in metabolic rate
with depth. The total effect upon metabolic
rate depends upon the relative effects of
temperature and pressure at those combinations of the two factors that the animals
actually encounter in that part of the
Contribution No. 2680 from the Woods Hole
Oceanographic Institution and No. 112 from the
Bermuda Biological Station. This work was supported by National Science Foundation grants
GB 7355 and GB 16161 and a grant from the Ber-
muda Biological Station.
ocean in which they live.
We have previously shown (Teal and
Carey, 1967) that the effects of pressure on
the respiration of epipelagic euphausids is
negligible in the ocean. Their respiratory
rate is determined almost solely by the
temperatures they encounter in their migrations. However, one mesopelagic euphausid behaved differently in that it
maintained a constant respiratory rate over
its natural depth range. Napora (1964)
indicated that Systellaspis debilis, a mesopelagic caridean crustacean, also had a
constant respiratory rate throughout its
vertical range in the ocean.
We have extended these observations on
mesopelagic Crustacea to include, besides
Systellaspis debilis which we tested again,
three more carideans: Oplophorus spinosus, Parapandalus richardi, and Acanthephyra purpurea, and one penaeid, Sergestes crassus. In all these animals the effect
of pressure is to stimulate respiration so as
to counteract the effect of decreasing temperature with depth and to maintain respiration at an approximately constant level
throughout the vertical range of the animals.
METHODS
p a r t o f the d a t a were o b t a i n e d at the
T>___, I T>- I • I o.. ..•
•
i_ r> ,-r,
B e r m u d a Biological Station using the R/V
Panulrius
571
for collecting in nearby deep
572
JOHN M. TEAL
TABLE 1. Number of experiments (N) and probabilities (P) of pressure effects on scattering layer decapods.
5°
Temperature
Atmospheres
N
Systellaspis debilis
Q u = 2.5
Avg. wt. 0.8 g
1
1-51
51-101
6
15
14
Oplophorus spinosus
Q,o = 2.1
Avg. wt. 0.4 g
Parapandalus richardi
Qio = 2.1
Avg. wt. 0.2 g
AcanthepliA/ra purpurea
Q.o=2
Avg. wt. 1.7 g
Sergestes crassus
Ql0=1.9
Avg. wt. 0.3 g
1
1-51
51-101
1
1-51
51-101
18
23
22
4
15
12
C
15
10
1
1-51
51-101
3
7
IS
Species
1
1-51
51-101
10°
15°
20°
P
N
P
N
P
N
P
.008
.002
9
18
14
.001
.001
13
20
21
.10
.01
14
25
17
.07
.41
.11
.002
9
22
25
.03
.12
10
13
9
.03
.17
17
27
20
.02
.006
.004
.05
8
9
13
.03
.01
8
28
22
.001
.001
3
18
15
.001
.02
.006
.06
7
11
14
.09
.41
.008
.01
9
14
12
.03
.4
water. The remaining data was obtained
from Woods Hole Oceanographic ships in
the Sargasso. Animals were collected with a
two meter plankton net having 2 X 5 m m
mesh with a 20 liter plastic bucket on the
cod end. From sunset to midnight, tows of
20 to 40 minutes duration were made in
the upper 200 m. Occasionally, animals
were caught in deeper tows made for other
purposes and were used. Adult specimens
in good condition were selected, placed in
plastic dishes, and stored in a 10°C refrigerator overnight. The experiments
were done the following morning. No distinction was made between sexes. Occasionally, animals were kept for several
days, but most experiments were performed with those caught the previous
night. Experiments were all done on single
individuals and lasted from 90 minutes to
6 hours.
The specimens were brought to the experimental temperature at a rate of about
5°C/hr. They were then placed in chambers containing from 40 to 280 ml fresh sea
water which had been filtered through
0.45 ix Millipore niters and re-aerated. After an initial period, during which activity
and respiration declined rapidly, respiration was calculated from the decrease in
ox) gen within the chamber. Oxygen was
measured continuously with oxygen elec-
11
13
12
8
23
21
.05
.006
.5
.5
4
4
3
9
.006
trodes made according to Kanwisher
(1959).
The pressure apparatus was that used in
previous studies of euphausids (Teal and
Carey, 1967), and the procedure followed
was identical. Pressure was alternated between 0 and 50 atmospheres gauge pressure or 50 and 100 atmospheres at a single
temperature for periods of 15 to 60 minutes, long enough to get a valid respiration
rate. Rates were also measured at one
atmosphere in a darkened water bath with
animals individually placed in 250 ml
flasks. In these cases, observations of activity were made while measuring respiration.
In the pressure experiments, only respiration or activity could be measured, not
both simultaneously. The probability of an
effect of pressure was calculated from the
null hypothesis that, if there were no
effect, the group of experiments which
showed an increase in rate following an
increase in pressure would equal the group
showing a decrease in rate. Experiments
in which no change could be detected were
classed with the smaller group, and the
result compared with the binomial distribution. This calculation provides a
probability that there is an effect of pressure. The magnitude of the effect must be
judged from the standard errors about the
means which are plotted in the figures.
573
PRESSURE EFFECTS OF RESPIRATION
RESULTS
Visual observations showed that Systellaspis debilis reacted to changes in pressure
800
1200 -
101 Atm
200
51
FIG. 1.
101 Atm
800
101 Atm
by swimming actively for a period of a
few seconds to about ten minutes. They
then returned to their previous state which
we judged to be about the level of activity
necessary to keep the animal at one level
in the water, neither rising nor sinking.
The Qio's for the species tested (Table
1) averaged a little above two without any
distinguishable trend between species that
could be correlated with their ecology.
In almost all cases, there was a significant increase in respiration with increases
in pressure (Table 1). Most of the excep-
51
FIG. 4.
101 Atm
574
JOHN M. TEAL
800
6003
mm Oz
gmhr
400
-
200
r
1
i
51
FIG. 5.
FIGS. 1-5: Respiration of vertically migrating decapods at four temperatures and three pressures.
Dashed line indicates respiration versus depth in
the ocean neglecting the pressure effect; dotted line
includes pressure effect. For Systellaspis data
from Napora is shown at top of figure.
tions occurred at the higher temperatures,
but there was a notable lack of pressure
sensitivity in the case of Sergestes at 10 and
15°C.
Results are plotted in Figures 1-5 as respiration versus pressure at each of the four
temperatures used. Pressure in the ocean
corresponds to depth in the ratio of one
atmosphere to 10 m. There are also characteristic temperatures found at each
depth in the Sargasso, so that a given pressure corresponds to a definite temperature.
The actual temperatures we have used are
indicated in Figure 6 and are taken from
a temperature profile for January. Superimposed on each set of data in Figures 1-5
is a dashed curve showing how respiration
for that species would have varied with
depth if its rate were determined solely by
the temperature found at that depth. The
dotted line adds the effect of perssure. The
distance between the dotted and dashed
line shows the effects of pressure upon respiration in the ocean. From the surface to
a depth of between 500 and 700 m, the
respiration of all five species remains approximately constant. Below that depth,
1000
FIG. 6: Respiration of vertically migrating decapods in the Sargasso. Systellaspis debilis (S.d.),
Acanthephyra purpurea (A.p.), Sergestes crassus
(S.c), Oplophorus spinosus (O.s.), Parapandalus
richardi (P.r.). Dashed line is respiration of euphausid Thysanopoda tricuspidata (Teal and
Carey, 1967). N - position of nighttime population
maximum, D - daytime population maximum from
Fox ton (1970).
i.e., at lower temperatures, the pressure
effect is less and the respiratory rate declines.
DISCUSSION
Our results are considerably lower (Fig.
1) than those of Napora (1964) for Systellaspis though they are similar to those
found by Pearcy and Small (1968) using
Sergestes similis. Napora placed his animals in bottles and submerged them in the
ocean to subject them to high pressure.
Respiration was calculated from oxygen
concentration measured at the beginning
and end of the experiment. The higher
values found are perhaps attributable to
his technique for he had no way to allow
for the initially high respiration which we
found after the animals had just been handled. Our animals were in good condition
at the end of an experiment and could be
kept alive for days afterward. The experiments did not cause the change from
transparent to opaque appearance of the
575
PRESSURE EFFECTS OF RESPIRATION
TABLE 2. Comparison of oxygen consumption with depth on the basis of two hypotheses for
respiration rate versus calculated oxygen use in the water column from Siley {1951).
Depth
(meters)
200
400
600
800
1000
1200
Calculated
oxygen use
(Riley)
(mm'/l yr)
Respiration
(Childress, 1969)
(mm 3 /l y r )
This study
210 mm'/l yr
15 mm.yi yr
24 mrnVl yr
50
33
28
13
5
flesh that occurs before death in planktonic Crustacea. Thus, we do not believe that
our lower values were due to the use of
moribund animals.
The more important result, that the respiration of all the mesopelagic Crustacea
which have been investigated remains approximately constant throughout the depth
range through which the animals migrate (Fig. 6), is in agreement with that
of Napora (1964). Pearcy and Small
(1968) could demonstrate no effect of
pressures up to 50 atmospheres on the respiration of Sergestes similis. Their experiments were done below 10°C, and their
animals from the Pacific coast are from
waters that show less thermal variation
with depth than the waters from which
our animals were taken. We also found no
effect of pressure on Sergestes crassus under certain conditions, although the general result that pressure effects tend to make
respiration constant with depth remains
the same. There is some variation in respiration with depth, and this would change
somewhat depending upon what temperature-depth curve was used in the plot.
These differences would be slight for this
property changes very little, even seasonally, in the Sargasso where these animals
were collected. Figure 6 has a dashed line
showing the respiration versus depth of an
epipelagic euphausid (Teal and Carey,
1967) as an example of how respiration
changes in an animal where pressure has
little effect.
The difference between the decapods
and epipelagic euphausids is striking. The
euphausids are almost entirely unaffected
by pressures at the low temperatures at
6
3
3
0.8
0.3
11
16
23
9
5
which they encounter high pressures, and
their metabolism slows greatly during their
daytime hours in deep cold water. We
calculated that they save energy by this
slowing of metabolism in spite of the effort
of making the twice daily migration. The
decapods' metabolism is so arranged that
the effects of decreasing temperature are
offset by an equal and opposite effect of
pressure. This pattern also occurred in the
one mesopelagic euphausid on which we
previously reported (Teal and Carey,
1967).
All these mesopelagic animals are predaceous. They do not rise into the surface
layers but only to about 200 m at night
(Foxton, 1970). During both day and
night, they remain below the maximum
concentration of epipelagic animals, from
which they get a major part of their food.
This suggests that these predators feed on
the less active individuals of their prey,
those slightly lower in the water column, a
similar situation to that found in many
terrestrial predators. (In this position they
would also be best able to catch and swallow fecal pellets before they break up.)
But while the epipelagic forms may take
advantage of the lower temperatures they
encounter at depth to reduce their metabolism and save energy, the mesopelagic
forms perhaps cannot afford a similar
course of action. The biomass in the ocean
decreases logarithmically with depth
(Banse, 1964) so these mesopelagic forms
have much less food available to them
than do the epipelagic forms. The food is,
however, in larger pieces (larger animals)
and perhaps easier to catch in the slightly
deeper layers. Because there is less food
576
JOHN M. TEAL
available, the mesopelagic animals must be
ready to capture it throughout the 24
hours and throughout their vertical depth
range. Thus, they have evolved a mechanism which keeps their metabolism at a constant level regardless o£ the pressure and
temperature changes they experience.
There may well be a contrast between the
mesopelagic animals that are stimulated by
high pressure or by rises in pressure and
deeper animals that do not show such
stimulation (Macdonald el. a]., 1971).
Childress (1969) reported that in animals
from progressively greater depths the metabolism is reduced in relation to size by
means of a progressively more watery body
construction. "We suspect that this reduction in metabolic rate becomes important
only below the depth characterized by the
mesopelagic animals. We have compared
our data and that of Childress with the
calculations for oxygen consumption in the
Sargasso (Riley, 1951). Values for plankton volume versus depth were taken from
the same paper. Our respiration values
were calculated on the basis of a respiration rate of 250 mm3/gm hr. The results
(Table 2) show that respiration rates
from Childress, assuming a steady decrease
in metabolism with depth, account for
only about \0fo of the respiratory oxygen
consumption between 200 and 1200 m. Respiration calculated on the basis of a constant respiration with depth using our decapod value, account for only 10% of
Riley's value at 200 m but increase to 50%
by 600 m and 100% between 600 and 1200
m. The assumption of constant respiration
with depth seem to be in more reasonable
agreement with the calculations throughout the mesopelagic zone. The respiration
in the upper layers is due mostly to ani-
mals of the epipelagic, which being on the
average considerably smaller than our decapods, would be expected to have considerably higher respiration rates than the
typical decapod value we used in our calculation.
We think our results show a reasonable
picture of a mesopelagic community of active predatory animals moving just under
prey in vertical migrations and evolving a
metabolism that enables them to remain
active throughout their habitat by using
the stimulatory effect of increasing pressure upon their metabolism to offset the
depressant effect of decreasing temperature.
REFERENCES
Base, K. 1964. On the vertical distribution of
zooplankton in the sea. Progr. Oceanogr.,
2:53-125.
Childress, J. J. 1969. The respiratory physiology of
the oxygen minimum layer mysid, Gnatliophausia ingens. Ph.D. Thesis, Stanford Univ.,
Palo Alto, Calif.
Foxton, P. 1970. The vertical distribution of pelagic decapods (Crustacea: Natantia) collected on
the Sond cruise 1965. 1. The Caridea. J. Mar.
Biol. Ass. U.K. 50:939-960.
Kanwisher, J. W. 1959. Polarographic oxygen electrode. Limnol. Oceanogr. 4:210-217.
Macdonald, A. G., I. Gilchrist, and J. M. Teal.
1971. Some observations on the tolerance of
oceanic plankton to high hydrostatic pressure. J.
Afar. Biol. Ass. U.K. (In press)
Xapora, T. A. 1964. The effect of hydrostatic pressure on the prawn Systellaspis debilis. Narragansett Mar. I_al>. Occ. Publ. 2:92-94.
Pearcy, W. G., and L. F. Small. 1968. Effects of
pressure on the respiration of vertically migrating crustaceans. J. Fish. Res. Bd. Can.
25:1311-1316.
Riley, G. A. 1951. Oxygen, phosphate and nitrate
in the Atlantic Ocean. Bull. Bingham Oceanogr.
Collect. Yale Univ. 13:1-126.
Teal, J. M., and F. G. Carey. 1967. Effects of
pressure and temperature on the respiration of
euphausids. Deep-Sea Res. 14:725-733.