Intragel oxygen promotes hypoxia tolerance of scyphomedusae
1 Laboratory One, The Evergreen State College, Olympia, Washington 98505,
USA
2 Academia Cotopaxi, Casilla 17-01-199, Quito, Ecuador
3 Alfred Wegener Institute for Polar and Marine Research,
Columbusstraße 27568 Bremerhaven, Germany
* Author for correspondence (e-mail: thuesene{at}evergreen.edu)
Accepted 19 April 2005
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: critical partial pressure, gel, hypoxia, jellyfish, metabolic rate, oxyregulation, scyphomedusae
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Pelagic organisms such as shrimps, cephalopods and fishes that can easily
move in and out of low oxygen conditions typically tolerate hypoxia through
primarily aerobic metabolic adaptations
(Childress and Seibel, 1998),
therefore the existing paradigm suggests that estuarine medusae should also
live in hypoxia through aerobic adaptations. A study on the enzymatic
activities of medusae found that both hydromedusae and scyphomedusae lack
several of the -opine dehydrogenases, suggesting they lack much anaerobic
capacity (Thuesen and Childress,
1994
). These enzymes are typically used by invertebrates when
tolerating low oxygen conditions
(Hochachka and Somero, 2002
)
and are present in sea anemones (Walsh,
1981
) that experience episodic night-time hypoxia in tide pools.
To investigate the hypothesis that medusae live in hypoxia by means of aerobic
adaptations, we measured the mass-specific oxygen consumption rate
(
O2) under
declining oxygen concentrations and determined the critical partial pressure
of oxygen (Pcrit) on Aurelia labiata and three
other species of scyphomedusae. Measurements of intragel oxygen content were
taken to begin elucidating the role of gelatinous tissue in medusan
physiology, and laboratory experiments were conducted to determine the
influence of oxygen conditions on the behaviour of A. labiata.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Oxygen measurements
Oxygen measurements made during experiments on C. quinquecirrha
from Chesapeake Bay used a PreSens Microx 8 oxygen meter (Precision Sensing,
GmbH, Germany); however, all other oxygen measurements in this study were made
using a fibre optic oxygen optode connected to a PreSens Microx TX3
temperature-compensated oxygen meter (Precision Sensing, GmbH, Germany). Type
B2-NTH optodes were housed in 80 mm stainless steel needles. Optical fibres
had probe tips 55 µm in diameter. Respiration experiments were carried
out in glass chambers containing FSW (0.2 µm filter, containing 50 mg each
of streptomycin and ampicillin) and kept in the dark at a constant temperature
on an orbital shaker at 85 r.p.m. to facilitate mixing in the respiration
chambers. Experiments were continued until specimens exhausted all of the
oxygen in the respirometry chamber or had ceased to consume oxygen. For
intragel oxygen profiles, specimens of A. labiata were harnessed to
paraffin platforms in open chambers of well-stirred FSW (10 µm filter)
using dome-shaped harnesses constructed of tempered 0.222 mm nylon netting.
Oxygen optodes were inserted through a 1 cm circular opening in the top of the
harness using a Narishige, Tokyo, Japan micromanipulator while viewing
specimens under a dissecting microscope. Intragel oxygen measurements on
unharnessed specimens were also taken at the surface of open cylindrical tanks
under five oxygen conditions: normoxia, hypoxia (30% air saturation), anoxia
(for 1 h and 2 h) and anoxia followed by a recovery period (2 h in anoxia
followed by 2.5 h in normoxia). Specimens were allowed to swim freely during
the incubation period; afterwards, optodes were inserted by hand into
specimens restrained against the clear acrylic tanks until oxygen measurements
stabilised (
1 min). Oxygen measurements were made in three easily
replicated locations: the aboral subsurface gel, the mid-point of the mesoglea
and the gonad (Fig. 1).
|
Data analysis
Oxygen consumption rates were compared using two-tailed t-tests.
Linear regression was used to determine Pcrit. Comparisons
of behavioural data were made using analysis of variance (ANOVA) followed by a
Fisher PLSD post-hoc analysis. The possible influence of animal size
on intragel oxygen comparisons was checked using multivariate ANOVA (MANOVA)
with diameter as the size parameter, and comparisons of intragel oxygen
partial pressures were also performed using MANOVA. The SPSS general linear
model MANOVA was evaluated using Pillai's Trace statistic followed by Dunnett
T3 post-hoc analyses for data sets with unequal variances. All other
analyses were performed using the Statview II computer program. Significance
was determined at P<0.05.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
Intragel oxygen
Oxygen concentrations through the gel of A. labiata were measured
on 25 harnessed specimens. Striking differences were seen between profiles
made in the aboral to oral direction and those in the oral to aboral
direction, and typical examples are shown in
Fig. 3. In specimens harnessed
with the oral side down, the upper section of the exumbrellar gel displays a
typical Fickian diffusion gradient (Crank,
1975). The diffusion gradient intensifies in the subumbrellar
region of the medusa due to increased tissue heterogeneity and metabolic use
of intragel oxygen. In specimens harnessed with the oral side up, oxygen
supply through the outer bell surface was almost entirely eliminated, oxygen
content was lower, and the oxygen profile of the mesoglea was reversed
(Fig. 3). The similarities in
intragel oxygen contents between specimens harnessed with the aboral side down
(Fig. 3) and unharnessed
specimens held in hypoxia and anoxia (Fig.
4) demonstrate that intragel oxygen concentration was affected
within the time frame of the harnessing preparation (
1 h). Gel becomes
depleted of oxygen within the time it takes to harness the specimen and align
the probe as animal metabolism consumes oxygen and exumbrellar oxygen
diffusion is repressed. These profiles demonstrate clearly that diffusion from
the subumbrellar cavity by itself is insufficient to supply oxygen to the
metabolically active tissues of the organism, and jellyfish must be using
intragel oxygen to meet their metabolic needs.
|
|
Intragel oxygen experiments demonstrated the capacity of Aurelia
labiata to use intragel oxygen as a reservoir to support its metabolic
needs when it migrates from higher oxygen waters into low oxygen waters
(Fig. 4). Using bell diameter
as the size parameter, there was no effect of size on the intragel comparisons
(MANOVA, P>0.20). Intragel oxygen becomes significantly reduced in
the bell surface, mid-gel and gonad tissues after 1 h in hypoxia (30% air
saturation, N=7) and anoxia (N=4)
(Fig. 4, MANOVA,
P<0.001; Dunnett T3 post-hoc analyses,
P<0.02). However, the oxygen content in the midgel and gonad
tissues were not significantly different between the hypoxia and 1 h anoxia
treatment (Fig. 4; Dunnett T3
post-hoc analyses, P>0.05). After 2 h in anoxia
(N=6), gel oxygen reached environmental levels
(Fig. 4). When specimens that
had been held for 2 h in anoxia were transferred to normoxic seawater,
intragel oxygen recovered to 70% of normal after 2.5 h (N=4),
but oxygen contents in all three tissues still remained significantly lower
than in specimens in normoxia (Fig.
4, MANOVA, P<0.001; Dunnett T3 post-hoc
analyses, P<0.001). When A. labiata is transferred to
lower oxygen environments, oxygen is depleted from the exumbrellar surface due
to the reversal of the direction of oxygen diffusion, and the mesoglea
continues to supply oxygen to metabolically active tissues.
Behaviour experiments
Aurelia labiata displayed different behaviour patterns under
different oxygen regimes in the laboratory
(Fig. 5). In air-saturated,
hypoxic and anoxic tanks, A. labiata typically swims against the tank
bottom or water surface with occasional vertical up and down forays. In
stratified oxygen conditions, A. labiata travels the greatest
distance as it swims back and forth through the oxycline. The vertical
distance that A. labiata travelled while swimming in the stratified
oxygen conditions was significantly higher than the other conditions (ANOVA,
Fisher's PLSD, P<0.01, Fig.
6A). The time spent swimming was not significantly different in
the tanks with oxygen, but swimming period was significantly reduced in anoxia
(ANOVA, Fisher's PLSD, P<0.01,
Fig. 6B). The apparent
contradiction between distance travelled
(Fig. 6A) and time spent
swimming (Fig. 6B) can be
explained due to the individuals that were actively swimming against either
the surface or bottom of the normoxia and hypoxia tanks
(Fig. 5). Aurelia
labiata is least active when under anoxia, and bell pulsation rate was
significantly reduced in the anoxia tanks (ANOVA, Fisher's PLSD,
P<0.01, Fig.
6C).
|
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The critical oxygen partial pressures for the medusae of these four species
of Scyphozoa and our behavioural observations indicate that they can endure
all but the most severely hypoxic environments without undergoing any major
metabolic transition to anaerobiosis. Other recent observations indicate that
some species of hydromedusae (Rutherford
and Thuesen, 2005) and ctenophores
(Thuesen et al., 2005
) can
also tolerate very low oxygen conditions. However, some hydromedusae displayed
oxyconformation and had higher Pcrit values than the
scyphomedusae in this study (Rutherford
and Thuesen, 2005
). The ability of scyphomedusae to function
aerobically is similar to that displayed by pelagic crustaceans
(Childress, 1975
;
Cowles et al., 1991
),
cephalopods (Seibel et al.,
1997
) and fishes (Torres et
al., 1979
) in the midwater oxygen minimum layer off California,
where oxygen partial pressures below 30 hPa persist over millennia
(Childress and Seibel,
1998
).
Intragel oxygen
The majority of the metabolically active tissues of scyphomedusae is
sandwiched between the largely acellular gel of the aboral mesoglea and the
seawater of the subumbrellar space, and we investigated whether overlying gel
supports oxygen diffusion to these metabolically active tissues. Scyphomedusae
swim through sustained contractions of the subumbrellar musculature and the
myofibril layer of this muscle tissue is heavily interdigitated with the
mesogleal gel (Gladfelter,
1972; Anderson and Schwab,
1981
). These myofibrils contain neither microtubles nor
sarcoplasmic reticulum, and it has been proposed that the mesoglea must be
directly responsible for supplying calcium to the myofibril cells
(Anderson and Schwab, 1981
).
Our intragel oxygen measurements indicate that the mesoglea is also supplying
oxygen to the musculature and other metabolically active tissues in the
subumbrellar region. Nevertheless, in some large species of scyphomedusae, a
coronal swimming muscle also hangs free in the water of the subumbrellar space
(Russell, 1970
). This
indicates that there are limits on intragel oxygen supply to the subumbrellar
musculature, and oxygen supply may have been an important factor in the
evolution of medusan morphology.
Scyphomedusae can regulate their oxygen consumption down to very low oxygen
partial pressures due to the suite of diffusion gradients that exist between
the surrounding seawater and mesogleal gel with metabolically active tissues.
Oxygen diffusion gradients are described by Fick's first law:
F=DC/
x, where
F=transfer rate per unit area of section, D is the diffusion
coefficient, C is the oxygen concentration and x is the
space coordinate perpendicular to the section
(Crank, 1975
). If oxygen
declined in both the umbrellar gel and the subumbrellar seawater at the same
rate,
C across the subumbrellar tissue would be maintained and
F across these tissues would remain unchanged. The rate that oxygen
diffuses into subumbrellar tissue (F1) is dependent on the
magnitude of two general oxygen gradients. F2 is the
diffusion of oxygen from aboral surrounding seawater into mesogleal gel.
F3 is the gradient from oxygen in the subumbrellar
seawater into the oral mesogleal gel. As long as F2 and
F3 are both large enough to maintain oxygen partial
pressures in gel above those needed to support F1, the
jellyfish oxyregulates. If F2 or F3
fall below that level, the critical partial pressure of oxygen is reached, the
oxygen gradient is inadequate to allow sufficient oxygen to diffuse into the
tissue to meet aerobic metabolic demand, and a transition to anaerobiosis
would be expected (Grieshaber et al.,
1988
).
Behaviour under different oxygen conditions
The observations of the behaviour of Aurelia labiata made in
normoxia are similar to those made in much larger tanks
(Mackie et al., 1981).
Aurelia labiata is not as active in anoxia. When compared to the
other oxygen treatments, the visually apparent difference in the swimming
tracks of the medusae in oxygen-stratified tanks is striking
(Fig. 5). Although no
significant differences in the three behaviour parameters between specimens in
normoxia or hypoxia were observed, the distance traveled by specimens in 18%
air saturation (Figs 5 and
6) is slightly elevated. It
appears that 18% oxygen saturation is approaching a level of hypoxia that
begins to induce behavioural changes. Experiments conducted at 30% air
saturation used animals that were starved prior to observations, and this
conditioning also complicates definitive interpretation of these behavioural
data. Nevertheless, these experiments demonstrated that the acute threshold
for provoking behavioural changes in A. labiata is somewhere near its
Pcrit and that oxygen stratification stimulates swimming
across the oxycline.
Our laboratory observations of the behaviour of A. labiata in
stratified tanks are in agreement with those made on the distribution of
Chrysaora quinquecirrha in oxygen-stratified areas of Chesapeake Bay
(Keister et al., 2000).
Stratified oxygen levels in eutrophic estuarine environments can have
pronounced impacts on the trophic interactions of planktonic organisms
(Breitburg et al., 1994
,
1999
). Stimulation of
intra-oxycline swimming behaviour by oxygen stratification may augment the
impact of scyphozoans on planktonic prey, since currents generated while
swimming also function to move prey items within the tentacle capture zone of
medusae (Costello and Colin,
1994
). Breeding aggregations
(Hamner et al., 1994
) of
Aurelia labiata occur in the near-surface seasonal oxycline in
southern Puget Sound where oxygen concentrations range from 20% to 150% air
saturation over a distance of just 2.0 m (P.L.B. and E.V.T., manuscript in
preparation), and successful transfer of sperm in breeding aggregations of
A. labiata may also be promoted. Even in severe
(sub-Pcrit) hypoxia, A. labiata has sufficient
oxygen in its gel to support aerobic metabolic needs for up to several hours,
and this study suggests that jellyfish will only be affected by hypoxia when
they swim into waters with oxygen concentrations below their
Pcrit and remain there for over several hours.
Role of gel in jellyfish biology
The great diversity of histological characteristics of mesoglea has been
recognized for many years (Kölliker,
1865). In jellyfish, its primary role is usually considered to be
that of a supporting tissue. It provides hydrostatic skeletal support for
musculature (Alexander, 1964
;
Chapman, 1966
) and supports the
development of complex tissues (Schmid et
al., 1991
). Gel may also be an energy storage tissue, albeit a
poor one, and it can provide energy to metabolically active tissues during
periods of starvation (Hamner and Jenssen,
1974
). The internal gel milieu is a dynamic environment. It
accommodates buoyancy changes due to salinity shifts
(Mills, 1984
;
Wright and Purcell, 1997
), and
gel likely provides important ions to musculature
(Anderson and Schwab, 1981
). We
now know that gel also plays a key role in supporting oxygen delivery to
tissues. Jellyfish were some of the first mobile metazoans, and they evolved
in early seas with low oxygen levels
(Brenchley and Harper, 1998
).
Our study suggests that the evolution of gelatinous tissue that supports
oxygen diffusion may have played a role in the success of pelagic cnidarians
in those early hypoxic oceans. Diffusion gradients in mesoglea represent the
first hurdles jumped in the evolution of oxygen delivery systems that are
found in more complex metazoan animals.
List of symbols and abbreviations
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Alexander, R. M. (1964). Visco-elastic properties of the mesogloea of jellyfish. J. Exp. Biol. 41,363 -369.
Anderson, P. A. V. and Schwab, W. E. (1981). The organization and structure of nerve and muscle in the jellyfish Cyanea capillata (Coelenterata; Scyphozoa). J. Morphol. 170,383 -399.[CrossRef]
Arai, M. N. (2001). Pelagic coelenterates and eutrophication: a review. Hydrobiologia 451, 69-87.[CrossRef]
Benovi, A., Lu
i
, D., Onofri, V.,
Peharda, M., Cari
, M., Jasprica, N. and
Bobanovi
-
oli
, S. (2000). Ecological
characteristics of the Mljet Island seawater lakes (South Adriatic Sea) with
special reference to their resident populations of medusae. Sci.
Mar. 64,197
-206.
Breitburg, D. L., Steinberg, N., Dubeau, S., Cooksey, C. and Houde, E. D. (1994). Effects of low dissolved oxygen on predation on estuarine fish larvae. Mar. Ecol. Prog. Ser. 104,235 -246.
Breitburg, D. L., Rose, K. A. and Cowan, J. H. (1999). Linking water quality to larval survival: predation mortality of fish larvae in an oxygen-stratified water column. Mar. Ecol. Prog. Ser. 178,39 -54.
Brenchley, P. J. and Harper, D. A. T. (1998). Palaeoecology: Ecosystems, Environments and Evolution. London: Chapman & Hall.
Brodeur, R. D., Sugisaki, H. and Hunt, G. L. (2002). Increases in jellyfish biomass in the Bering Sea: implications for the ecosystem. Mar. Ecol. Prog. Ser. 233,89 -103.
Chapman, G. (1966). The structure and functions of the mesogloea. Symp. Zool. Soc. Lond. 14,147 -168.
Childress, J. J. (1975). The respiratory rates of midwater crustaceans as a function of depth occurrence and relation to the oxygen minimum layer off Southern California. Comp. Biochem. Physiol. 50A,787 -799.[CrossRef]
Childress, J. J. and Seibel, B. A. (1998). Life
at stable low oxygen levels: adaptations of animals to oceanic oxygen minimum
layers. J. Exp. Biol.
201,1223
-1232.
Childress, J. J. and Thuesen, E. V. (1993). Effects of hydrostatic pressure on metabolic rates of six species of deep-sea gelatinous zooplankton. Limnol. Oceanogr. 38,665 -670.
CIESM (2001). Gelatinous Zooplankton Outbreaks: Theory and Practice. CIESM Workshop Series, no.14 , 112pp. Monaco: CIESM, Commission Internationale pour l'Exploration Scientifique de la mer Méditerranée.
Costello, J. H. and Colin, S. P. (1994). Morphology, fluid motion and predation by the scyphomedusa Aurelia aurita.Mar. Biol. 121,327 -334.[CrossRef]
Cowles, D. L., Childress, J. J. and Wells, M. E. (1991). Metabolic rates of midwater crustaceans as a function of depth of occurrence off the Hawaiian Islands: Food availability as a selective factor? Mar. Biol. 110,75 -83.[CrossRef]
Crank, J. (1975). The Mathematics of Diffusion. London: Oxford University Press.
Dawson, M. N. and Hamner, W. M. (2003). Geographic variation and behavioral evolution in marine plankton: the case of Mastigias (Scyphozoa, Rhizostomeae). Mar. Biol. 143,1161 -1174.[CrossRef]
Gladfelter, W. B. (1972). Structure and function of the locomotory system of the scyphomedusa Cyanea capillata.Mar. Biol. 14,150 -160.[CrossRef]
Graham, W. M., Martin, D. L., Felder, D. L., Asper, V. L. and Perry, H. M. (2003). Ecological and economic implications of a tropical jellyfish invader in the Gulf of Mexico. Biol. Invas. 5,53 -69.[CrossRef]
Grieshaber, M. K., Kreutzer, U. and Pörtner, H. O. (1988). Critical PO2 of euryoxic animals. In Oxygen Sensing in Tissues (ed. H. Acker), pp.37 -48. Berlin: Springer-Verlag.
Gücü, A. C. (2002). Can overfishing be responsible for the successful establishment of Mnemiopsis leidyi in the Black Sea? Estuar. Coast. Mar. Sci. 54,439 -451.[CrossRef]
Hamner, W. M. and Jenssen, R. M. (1974). Growth, degrowth, and irreversible cell differentiation in Aurelia aurita.Am. Zool. 14,833 -849.
Hamner, W. M., Hamner, P. P. and Strand, S. W. (1994). Sun compass migration by Aurelia aurita (Scyphozoa)population retention and reproduction in Saanich Inlet, British Columbia. Mar. Biol. 119,347 -356.[CrossRef]
Hochachka, P. W. and Somero, G. N. (2002). Biochemical Adaptation: Mechanisms and Process in Physiological Evolution. New York: Oxford University Press.
Keister, J. E., Houde, E. D. and Breitburg, D. L. (2000). Effects of bottom-layer hypoxia on abundances and depth distributions of organisms in Patuxent River, Chesapeake Bay. Mar. Ecol. Prog. Ser. 205,43 -59.
Kideys, A. E. (1994). Recent dramatic changes in the Black Sea eco-system: the reason for the sharp decline in Turkish anchovy fisheries. J. Mar. Syst. 5, 171-181.[CrossRef]
Kideys, A. E. and Romanova, Z. (2001). Distribution of macrozooplankton in the southern Black Sea during 1996-1999. Mar. Biol. 139,535 -547.[CrossRef]
Kölliker, A. (1865). Icones Histologicae oder Atlas der vergleichenden Gewebelehre. Leipzig: Engelmann.
Larson, R. J. (1987). Respiration and carbon turnover rates of medusae from the NE Pacific. Comp. Biochem. Physiol. 87A,93 -100.[CrossRef]
Lynam, C. P., Hay, S. J. and Brierley, A. S. (2004). Interannual variability in abundance of North Sea jellyfish and links to the North Atlantic Oscillation. Limnol. Oceanogr. 49,637 -643.
Mackie, G. O. and Mills, C. E. (1983). Use of the Pisces IV submersible for zooplankton studies in coastal waters of British Columbia. Can. J. Fish. Aquat. Sci. 40,763 -776.
Mackie, G. O., Larson, R. J., Larson, K. S. and Passano, L. M. (1981). Swimming and vertical migration of Aurelia aurita (L) in a deep tank. Mar. Behav. Physiol. 7, 321-329.
Mangum, C. P., Oakes, M. J. and Shick, J. M. (1972). Rate-temperature responses in scyphozoan medusae and polyps. Mar. Biol. 15,298 -303.[CrossRef]
Mills, C. E. (1984). Density is altered in hydromedusae and ctenophores in response to changes in salinity. Biol. Bull. 166,206 -215.
Mills, C. E. (2001). Jellyfish blooms: are populations increasing globally in response to changing ocean conditions? Hydrobiologia 451,55 -68.[CrossRef]
Purcell, J. E., Breitburg, D. L., Decker, M. B., Graham, W. M., Youngbluth, M. J. and Raskoff, K. A. (2001). Pelagic cnidarians and ctenophores in low dissolved oxygen environments. In Coastal Hypoxia: Consequences for Living Resources and Ecosystems (ed. N. N. Rabalais and R. E. Turner), pp.77 -100. Washington, DC: American Geophysical Union.
Rabalais, N. N. and Turner, R. E. (ed.) (2001). Coastal Hypoxia: Consequences for Living Resources and Ecosystems. Coastal and Estuarine Studies No. 58. Washington, DC: American Geophysical Union.
Russell, F. S. (1970). The Medusae of the British Isles. II. Pelagic Scyphozoa with a Supplement to the First Volume on Hydromedusae. Cambridge: Cambridge University Press.
Rutherford, L. D., Jr and Thuesen, E. V. (2005). Metabolic performance and survival of medusae in estuarine hypoxia. Mar. Ecol. Prog. Ser. in press.
Schmid, V., Bally, A., Beck, K., Haller, M., Schlage, W. K. and Weber, C. (1991). The extracellular matrix (mesoglea) of hydrozoan jellyfish and its ability to support cell adhesion and spreading. Hydrobiologia 216/217,3 -10.[CrossRef]
Seibel, B. A., Thuesen, E. V., Childress, J. J. and Gorodezky,
L. A. (1997). Decline in pelagic cephalopod metabolism with
habitat depth reflects differences in locomotory efficiency. Biol.
Bull. 192,262
-278.
Shick, J. M. (1991). A Functional Biology of Sea Anemones. London: Chapman & Hall.
Thill, H. (1937). Zur Kenntnis der Aurelia.Zeitsch. wiss. Zool. 150,52 -96.
Thuesen, E. V. and Childress, J. J. (1994).
Oxygen consumption rates and metabolic enzyme activities of oceanic California
medusae in relation to body size and habitat depth. Biol.
Bull. 187,84
-98.
Thuesen, E. V., Rutherford, L. D., Jr and Brommer, P. L. (2005). The role of aerobic metabolism and intragel oxygen in hypoxia tolerance of three ctenophores: Pleurobrachia bachei, Bolinopsis infundibulum and Mnemiopsis leidyi. J. Mar. Biol. Assn. UK 85,627 -633.
Torres, J. J., Belman, B. W. and Childress, J. J. (1979). Oxygen consumption rates of midwater fishes as a function of depth of occurrence. Deep-Sea Res. 26A,185 -197.
Vernon, H. M. (1895). The respiratory exchange of the lower marine invertebrates. J. Physiol. Lond. 19, 18-70.
Walsh, P. W. (1981). Purification and characterization of two allozymic forms of octopine dehydrogenase from California populations of Metridium senile. J. Comp. Physiol. 143,213 -222.
Wright, D. A. and Purcell, J. E. (1997). Effect
of salinity on ionic shifts in mesohaline scyphomedusae, Chrysaora
quinquecirrha. Biol. Bull.
192,332
-339.
Related articles in JEB: