J. exp. mur. Biol. Ecol., 1971, Vol. 7, pp.

263-269; North-Holland

OXYGEN REQUIREMENTS

OF OCTOPUS

TEMPERATURES

Publishing Company, Amsterdam

BRZAREUS

Robson AT DIFFERENT

AND OXYGEN CONCENTRATIONS

KATARINA TOMLJENOVIC BORER and CHARLES E. LANE

Rosenstiel

School

of Marine

and Atmospheric

Science,

Unioersity

of Miami,

Miami,

Florida,

U.S.A.

Abstract: Oxygen consumption was determined polarographically

for Octopus briarerrs Robson
at 20 and 30 C and at different oxygen concentrations to investigate the ability of octopus to withstand changes in temperature and oxygen depletion during periodic confinement to small bodies
of water at low tide. Oxygen consumption was temperature dependent with mean rates of 0.0417
ml 0,/g/h. at 20 C and of 0.0911 ml 0,/g/h at 30 C for animals weighing 250-443 g. At both
temperatures 0. briareus regulates the rate of oxygen consumption by compensatory increase in the
rate of ventilation when the oxygen level falls below 2.8 ml O,/ I. The fresh sea-water requirements
of octopus at temperatures between 20 and 30 C have been calculated from the oxygen uptake data.

Octopus frequently
inhabits the intertidal
zone where periods of low tide may
confine it to small bodies of water of rapidly changing temperature
and oxygen
content. Many workers have documented the ability of octopods to maintain constant
oxygen consumption
when the oxygen content of sea water is varied (Henze, 1910;
Hazelhoff, 1938; Maginnis & Wells, 1969). The relationship
between environmental
temperature and oxygen consumption
in octopus has not been fully examined because
of difficulties inherent in controlling
the temperature
of open-circulated
sea water.
The measurements
of oxygen consumption
in octopus have generally been limited to
the temperatures

prevailing

when the studies were performed.

Oxygen consumption

was determined for Octopus cyanea at 24.5-27.5 C (Maginnis

& Wells, 1969), for
0. vulgaris at 15.5 C (Jolyet & Regnard, 1877), at 24 C (Montuori,
1913) and at
1 l-21 C during short-term exposure to rapidly changing temperature in uncirculated
sea water (Vernon, 1896).
We have examined the effects of a 10 C change in environmental
temperature
on
the oxygen consumption
in 0. briareus Robson using a temperature-controlled
apparatus for running sea water (Moore & Gray, 1969). The experimental temperatures
of 20 and 30 C were chosen as representing
the seasonal range of sea temperatures
at Miami; oxygen concentration
was monitored polarographically
in a closed system
I Contribution No. 1321, Rosenstiel School of Marine and Atmospheric Science, The University
of Miami.
* Present address: 1724 South University Avenue, Ann Arbor, Michigan, U.S.A.
263

264

KATARINA

which simulated

TOMLJENOVIC

the conditions

BORER AND CHARLES E. LANE

facing octopus

confined

to a small body of water at

low tide.

MATERIALS AND METHODS

Nine female 0. briureus Robson

captured

1969 when the mean water temperature

intertidally

in the Florida

Keys in October

was 26 C (range 24-27 C) were used. Their

mean weight was 345.6 g (250.@-443.0 g). A polyvinyl chloride pipe section closed
at one end withperforatedPlexiglass
measuring approximately 10 x 30cmwasprovided
for each animal. Before the start of separate experiments in January, February, and
March the ambient temperature
of sea water supplied to the animals was 19.3,
19.6, and 21.2 C, respectively.
Oxygen consumption
was measured in a closed system consisting
of a 12-litre
rectangular glass tank covered with a Plexiglass lid fitted with a polarographic
oxygen
probe (YSI Model 51) in a rubber stopper. The oxygen probe registered p.p.m.
(mg 0,/l) of oxygen. The sea water in the respiration chamber was mixed by a motordriven Teflon-coated
magnet. A perforated
Plexiglass partition
2.5 cm above the
tank bottom separated the rotating magnet from the major portion of the tank
occupied by the octopus. An opaque screen was placed between the respiration vessel
and the observer. An octopus vigorously resists efforts to displace it from its home
tank (Walker, Longo & Bitterman, 1970); the animals used in these experiments were
transferred to the test vessel with minimal handling. The pipe home containing
an
animal was lifted from the water and drained through the perforations in the Plexiglass
rear wall. The drained pipe and its contained octopus were weighed, and the animal
was then induced
above it.

to enter the respiration

chamber

by suspending

the inverted

pipe

Determinations
of oxygen concentration
were made every 30 or 60 set, and the
experiment was discontinued
when the oxygen content of the sea water fell to0.7-1.0 ml
02/1. The rate of ventilation
periment.

was measured

at 5-10 min intervals

during

each ex-

The temperature
of the circulating
sea water was maintained
(kO.5 C) by a
thermostatically-controlled
mixing valve (Moore
& Gray, 1969) admitting
appropriate amounts of ambient and heated or cooled sea water to the animals home
tank. Experiments
were conducted at 20 and 30 C. Each animal was acclimated to
the test temperature at a rate of 2 C/24 h and held at the test temperature for at least
24 h before being placed in the respiration
chamber. The oxygen probe was also
equilibrated
to the test temperature for at least 12 h before each test. The water temperature was measured at the beginning and at the end of the experiment. There was
an average of 1.4 C rise in temperature
of 20 C water, and a +0.2 C change in
temperature
of 30 C water during the course of an experiment. During the experiments the animals generally rested quietly on the tank walls, occasionally
shifting
their position and intermittently
probing the walls of the tank with the arm tips.

TEMPERATURE

EFFECTS

ON OCTOPUS

RESPIRATION

265

Fifteen determinations
of oxygen consumption
and ventilation
rates were made;
10 with eight individuals
at 20 C and 5 with four animals at 30 C. Three animals
were tested at both temperatures,

and one was tested twice at 30 C.

TABLE

Oxygen consumption

of Octopus briarem

at different temperatures.
30 C

20 C
Total oxygen
consumption

Octopus weight

(ml Wgih)

(8)

250.0
250.0
299.5
323.5
333.5
346.2
378.8
408.5
414.3
441.1

0.0533
0.0566
0.0242
0.0299
0.0454
0.0368
0.0258
0.0357
0.0499
0.0597

293.2
295.0
341 .o
366.3
443.0

344.5 mean

0.0417 mean

(8)

Total oxygen
consumption

Octopus weight

(ml G/g/h)
0.0909
0.0952
0.1011
0.1101
0.0582

._- _~ 347.7 mean

0.0911 mean

RESULTS

The oxygen consumption

was temperature

at 20 C and 0.0911 ml 0,/g/h

dependent

averaging

at 30 C. Table I gives individual

0.0417 ml 0,/g/h
and mean

oxygen

consumption
at 20 and 30 C calculated from the slopes of linear regressions. Based on
the mean rates of oxygen consumption
at 20 and 30 C the Q,, is 2.18, and
the temperature-dependent

increase

in the rate

of removal

of oxygen

per C is

0.0049 ml 0,/g/h.
Due to the opposing
(Table

effects of rising

water temperature

on oxygen

I), it took 80-182 min for 0. briareus to remove the available

consumption
oxygen to 0.7

ml 02/1 at 20 C and 37-47 min at 30 C (Fig. 1). At both 20 and 30 C the oxygen
removal rate tended to be constant throughout
the range of oxygen concentrations
in all animals as indicated by small scatter of the readings about the calculated linear
regressions.
Fig. 2 shows the effect of temperature
and of available oxygen on the ventilation
rate. As the available oxygen decreased from about 2.79 ml OJl to 0.7 ml OJl at
either 20 or 30 C there was a systematic increase in the ventilation rate of 0. briareus.
At both 20 and 30 C the rate of increase as a function of declining oxygen concentration was linear,

and the slopes of regression

lines were very similar,

namely,

-3.67

KATARINA

266

TOMLJENOVIe

BORER

AND

CHARLES

E. LANE

T 4.0 ..
E
Ii
0 3.0 -

60

30

90

120

MINUTES

Fig. 1. Oxygen depletion of sea water at 20 and 30 C by two Octopus briureus of comparable
(333.5 and 341.0 g), and the regression
lines from which the rates of oxygen consumption
calculated
(0.0454 ml 0*/g/h and 0.101 I ml 02/g/h respectively).

il

weight
were

0 2oc
l

3oc
/

,/

-6

. ,/
,

,/
,/
,/i
,
l

,.,:

9/
,I
,,/
,_, 0
0

,/

,.&

,/

,/

.q/o
,,,
0

p.P.m

Fig. 2. Ventilation

0,

rates of Ocropus briureus at 20 and 30 C and at different

oxygen

concentrations.

TEMPERATURE

EFFECTS ON OCTOPUS RESPIRATION

267

at 20 C and -3.94 at 30 C. This is an increase of about 4 ventilation cycles/min

for each 1 p.p.m. decrease in the concentration of oxygen below 2.79 ml 0,/l.
DISCUSSION

The rate of oxygen consumption of 0. briareus is dependent on temperature.

After a 24-h exposure to 20 C octopus removed oxygen at an average rate of 0.0417
ml 0,/g/h, while at 30 C the mean oxygen consumption was 0.0911 ml 0,/g/h
which gives a Q,, of 2.18, a value close to 2.2 obtained by Krogh (1914) for the Q,,
of metabolic rate of poikilotherms and ambient temperature.

-I

0.1 o-,
;
c
&
z=I;
v-a\
z
E
2 <005-

_.

I
0
d
0

A.

0
Z,
m0
>
;

Borer &Lane
Jolyet LRegnard
Maginnir &Wells
Montuori
Vernon

/
,/
0

10

,I

o
o
/
,/
,.,
d,?,
,,,

:
,,/
: /
,Y
..,(

. / i
l

,f

15
TEMPERATURE

20

2.5

30

(OC)

Fig. 3. Rates of oxygen consumption at different temperatures; 0 250-443 g Octopus briareus (present
study); A 2300 g 0. oulgaris (Jolyet & Regnard, 1877); n 280 g 0. uulgaris (Montuori, 1913);
0 7.1 g 0. uulgaris (Vernon, 1896); and 0 240412 g 0. cyunea (Maginnis & Wells, 1969): the
dashed line connects our mean values for 0, uptake of 0. briareus at 20 and at 30 C.

If oxygen consumption of three species of octopus is presented as a function of

temperature (Fig. 3), using the data of previous studies (Jolyet & Regnard, 1877;
Vernon, 1896; Montuori, 1913; Maginnis & Wells, 1969) the values fall along the
regression line for the mean values for 0. briareus at 20 and 30 C. The similarity
in oxygen uptake as a function of ambient temperature is remarkable in view of the
differences in analytical methods, temperature control, and acclimatization procedure. Although the values of Vernon (1896) fall somewhat below the expected
oxygen consumption for given temperature, he obtained a temperature-dependent
oxygen consumption between 11 and 21 C and a Q,, of 2.1 in a 7.1 g 0. vulgaris
exposed to a rapid 10 C gradient; Jolyet & Regnard (1877) using a single 2300 g
0. vulgaris obtained a value of the oxygen consumption at 15.5 C in agreement with
the present data.

268

KATARINA

Our data confirm

TOMLJENOVIC

earlier findings

BORER

AND

CHARLES

E. LANE

that over a wide range the oxygen consumption

is independent
of the oxygen content of sea water in octopods, e.g., Eledone moschata
(Henze, 1910) Octopus vulgaris (Hazelhoff, 1938) and 0. cyanea (Maginnis & Wells,
1969). As shown in Fig. 1, 0. briareus removed
rate from the available
30 C down

to about

concentrations
0.7 ml OJl,

oxygen from the sea water at a steady

of 4.2 ml 0,/l

at 20 C and 3.1 ml 0,/l

at which concentration,

at

0. cyanea also starts

showing signs of asphyxiation

(Maginnis & Wells, 1969).
Control of ventilation
rate appears to be one of the mechanisms involved in regulaVentilation
rate remained at about 21
tion of oxygen consumption
in octopus.
cycles/min until the oxygen content fell to about 2.79 ml OJl (Fig. 2). Between 2.8
ml OJl and 0.7 ml 02/1 0. briareus systematically
increased its ventilation
rate, at
both 20 and 30 C, by about 4 breathing cycles for every 1 p.p.m. drop in oxygen
concentration.
These findings indicate that 2.8 ml OJl is the lowest concentration
of oxygen that 0. briareus can tolerate without stress. Oxygen concentrations
below
2.8 ml OJl, alone or in conjunction
with the evolved COZ, appear to stimulate a
compensatory
increase in the ventilation
rate. Possibly the same stimulus may
induce attempts to escape described for animals receiving water of progressively
declining quality after it has passed through 3-4 preceding octopus tanks (Walker,
Longo & Bitterman, 1970). The relatively pronounced
influence of oxygen concentration on ventilation
rate in 0. briareus is in contrast to the results of Winterstein
(1925) who found insignificant
ventilation
changes in 0. vulgaris respiring in sea
water of declining oxygen content: using a cannulated-funnel
preparation
he found a
fourfold increase in respiratory volume as oxygen content fell to one fourth its original
level. Octopus probably
achieves a regulation
of oxygen consumption
through
TABLE II

Effect of temperature
on the oxygen consumption
water, and the volume of circulating

of Octopus briareus, the solubility of oxygen

sea water required to avoid hyperpnea.

Solubility of O2 at
salinities of 28.8-36.0 jO,,
Temp.
(0
20
21
22
23
24
25
26
27
28
29
30

Oxygen requirement
(ml 01/100 g/h)
4.2
4.1
5.2
5.7
6.2
6.1
1.2
7.1
8.2
8.7
9.2

(ml /I)
(from Harvey,
5.56-5.31
5.41-5.22
5.38-5.13
5.29-5.04
5.20-4.95
5.12-4.86
5.03-4.78
4.94-4.70
4.86-4.62
4.7774.54
4.68-4.46

1955)

in sea

Lower limit of
optimum
volumes of
circulating
sea
water (I/ 100 g/h)
1.26-1.32
I .37-i .43
1.49-1.55
1.61-l .68
I .73-l .8l
I .85-l .95
I .98-2.09
2.12-2.23
2.26-2.31
2.40-2.53
2.57-2.69

TEMPERATURE

EFFECTS ON OCTOPUS RESPIRATION

269

control of both ventilation rate and respiration volume, although only the former
was monitored in our experiments.
Using the figure of 2.8 ml 02/1 as the criterion of adequacy of circulating sea water,
and the solubility of oxygen in sea water at different temperatures (Harvey, 1955)
it is possible to calculate from our data the minimal volumes of fresh sea water that
will supply adequate oxygen to octopus without raising its rate of ventilation at
20 and 30 C (Table II): the opposing effects of temperature on the solubility of oxygen
and on the oxygen requirements of octopus demand an increase in the volume of
circulating sea water from 1.6 l/100 g octopus/h at 20 C to 2.69 l/100 g octopus/h
at 30 C.
ACKNOWLEDGEMENTS

We are grateful to Dr. Hilary B. Moore for the generous loan of the temperaturecontrol apparatus, and to Dr. Jay Zieman for the use of oxygen probe. The work was
supported in part by USPHS Grant HE-5489.

REFERENCES
HARVEY,H. W., 1955. The chemistry and fertility of sea waters. Cambridge University Press, Cambridge. 184 pp.
HAZELHOFF,E. H., 1938. tiber die Ausnutzung des Sauerstoffs bei verschiedenen Wassertieren.
Z. oergl. Physiol., Bd 26, S. 306-321.
HENZE, M., 1910. iiber den Einfluss des Sauerstoffdrucks auf den Gaswechsel einiger Meerestiere.
Biochem. Z., Bd 26, S. 255-278.
JOLYET,F. &P. REGNARD,1877. Recherches physiologiques sur la respiration des animaux aquatiques.
Arch. Physiol. norm. pathol., Ser. 2, T. 4, pp. 584-633.
KROGH,A., 1914. The quantitative relation between temperature and standard metabolism in animals.
Int. Z. physik.-them. Biol., Vol. 1, pp. 491-508.
MAGINNIS,L. A. & M. J. WELLS, 1969. The oxygen consumption of Octopus cyanea. J. exp. Biol.,
Vol. 51, pp. 607-613.
MONTUORI,A., 1913. Les processus oxydatifs chez les animaux marins en rapport avec la loi de
superficie. Arch. ital. Biol., T. 59, pp. 213-234.
MOORE, H. B. & M. K. GRAY, 1969. A temperature control system for running sea water. Special
Report, Institute of Marine Science, University of Miami, 10 pp.
VERNON,H. M., 1896. The respiratory exchange of lower marine invertebrates. J. Physiol., London,
Vol. 19, pp. 18-70.
WALKER, J. J., N. LONGO,& M. E. BITTERMAN,
1970.The octopus in the laboratory: handling,
maintenance, training. Beh. Res. Meth. Instr., Vol. 2, pp. 15-18.
WINTERSTEIN,H., 1925. Uber die chemische Regulierung der Atmung bei den Cephalopoden. Z.
uergl. Physiol., Bd 2, S. 315-328.