Does feeding limit cardiovascular modulation in the Dungeness crab Cancer magister during hypoxia?
Department of Biological Sciences, UNLV, 4505 Maryland Parkway, Las Vegas, NV 89154-4004, USA and Bamfield Marine Sciences Centre, Bamfield, British Columbia, Canada VOR 1BO
e-mail: imcgaw{at}ccmail.nevada.edu
Accepted 24 September 2004
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Summary |
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Key words: Cancer magister, cardiovascular system, crab, digestion, feed, hypoxia, physiology, ventilation
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Introduction |
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The physiological responses of decapod crustaceans to hypoxia are well
documented. Most species exhibit a pronounced bradycardia in conditions of
dissolved oxygen decrease (McMahon,
2001). In a number of species, cardiac output is maintained or
even increases, driven by an increase in stroke volume
(McMahon and Wilkens, 1975
;
Wilkes and McMahon, 1982
;
Airriess and McMahon, 1994
;
Reiber, 1995
;
Reiber and McMahon, 1998
).
Regional haemolymph flows are more variable among species; individual organ
perfusion may increase or decrease depending on the species and the severity
of the hypoxic regime (Airriess and
McMahon, 1994
; Reiber and
McMahon, 1998
). Oxygen uptake is usually maintained down to a
critical oxygen tension (Pcrit), initially by an increase in
ventilation rate and later by internal compensatory mechanisms
(Wilkes and McMahon,
1982
).
All the crustaceans used for the above mentioned studies were starved prior
to and/or were not fed during experiments. This protocol is adopted since the
stimulatory effect of food ingestion on metabolic processes is well known
(Wang, 2001). Decapod
crustaceans are no exception; oxygen uptake increases immediately after
feeding, reaching maximal levels within 2.5-4 h
(Houlihan et al., 1990
;
McGaw and Reiber, 2000
;
Robertson et al., 2002
;
Mente et al., 2003
). Oxygen
uptake can remain elevated for up to 48 h
(Legeay and Massabuau, 1999
;
McGaw and Reiber, 2000
). Blood
flow is diverted to the muscles while feeding and to the digestive organs
thereafter (McGaw and Reiber,
2000
). However, in nature, organisms do not starve themselves
before encountering environmental perturbations. The question then arises as
to how an animal balances the simultaneous demands of these physiological
systems.
The Dungeness crab Cancer magister is a commercially important
species along the Pacific coast of North America. It inhabits sandy and muddy
bays and estuaries, where it can encounter hypoxic water as low as 1.2 kPa
(Airriess and McMahon, 1994;
Bernatis and McGaw, 2004
). Its
cardiovascular responses to hypoxia follow the typical decapod pattern, with
heart rate decreasing from 75 beats min-1 to 45 beats
min-1 in severe hypoxia. This bradycardia is coupled with an
increased stroke volume, leading to a slight increase in cardiac output
(Airriess and McMahon, 1994
). A
decreased heart rate aids diastolic filling time, the trade off between
reducing heart rate and increasing stroke volume may be energetically
advantageous as well allowing increased perfusion pressures of arterial
systems (Reiber and McMahon,
1998
). The majority of this maintained cardiac output is shunted
via the sternal artery to the scaphognathite muscles, which aids the increase
in ventilatory frequency. The redistribution of blood through the sternal
artery may also protect the CNS from the effects of hypoxic exposure
(Airriess and McMahon, 1994
).
Thus, these alterations in cardiovascular variables enhance the ability of
Cancer magister to cope with hypoxia
(Airriess and McMahon, 1994
).
However, these experiments were performed on starved animals. Digestive
processes will pose an additional burden on animals already attempting to
supply adequate amounts of oxygen to the tissues. Therefore, the present study
sought to determine how feeding and subsequent digestion affect the ability of
Cancer magister to maintain cardiac function and balance tissue
perfusion in low oxygen tension environments.
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Material and methods |
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During experiments, crabs were held in a circular tank of 32 cmx30 cm
diameterxdepth in aerated running seawater at 10-12°C, with a layer
of sand lining the bottom. The tips of the chelae were glued together to
prevent the crabs from cutting the catheters, other than this they were able
to move freely. The crabs were allowed to settle for 12 h in the chamber
before experimentation. Data for cardiac and ventilatory parameters were
recorded continuously using an ADInstruments data acquisition system. All
recordings were carried out in constant dim light, which helped reduce any
nocturnal activity. The entire apparatus was surrounded by black plastic
sheeting to avoid visual disturbance to the animal. Hypoxic conditions
(3.2±0.2 kPa) were initiated by bubbling a mixture of nitrogen and air
into the water using a GF3/MP gas mixing pump (Cameron Instruments, Port
Aransas, TX, USA); oxygen levels were checked with an oxygen meter (YSI 55,
Yellow Springs, OH, USA). New steady states of dissolved oxygen were reached
in the experimental apparatus within 15-20 min and did not vary by more than
0.2 kPa during the experiments. A hypoxic regime of 3.2 kPa was used since it
approximated to the lowest oxygen tension at which the crabs would feed
(Bernatis and McGaw, 2004). For
feeding, a polyethylene tube (PE160) was inserted into the oesophagus and held
in place with dental dam. This allowed a liquefied fish meal, 2% of the crab's
body mass, to be administered at a rate of approximately 5 ml
min-1. It also helped reduce changes in physiological parameters
(apparent specific dynamic action) associated with food handling
(Carefoot, 1990
).
Three separate experiments were carried out. In the first experimental series, cardiovascular parameters of eight Dungeness crabs were monitored for 3 h in normoxia. The animals were then fed and monitored for a further 12 h in normoxia. In a second series of experiments, cardiovascular parameters of eight crabs were monitored for 3 h control period in normoxia. The animals were fed and then 1 h after feeding, hypoxia (3.2 kPa) was initiated for a total time of 6 h. Normoxic conditions were then restored for a further 6 h. In a final series of experiments eight crabs were monitored in control conditions for 3 h. Hypoxia (3.2 kPa) was then initiated and 3 h later the crabs were fed. Changes in cardiovascular parameters were recorded for a further 6 h in hypoxia, after which, normoxic conditions were restored for an additional 6 h. This time course of hypoxic exposure was chosen to emulate naturally occurring conditions based on the tidal cycle in Barkley Sound, British Columbia.
Haemolymph L-lactate levels (N=7) were measured during feeding in hypoxia. At set intervals the crabs were quickly removed from the tank (separate crabs were used at each time interval). Within 10 s, a 50 µl sample of haemolymph was withdrawn from a pereiopod artery at the base of the walking legs using needle and syringe. The sample was immediately frozen at -80°C to avoid degradation of compounds. L-Lactate levels of a 6 µl sample were later analysed using a Pointe Scientific (Canton, MI, USA) UV lactate test kit, with absorbance read at 550 nm (Spectra-Max Plus, Molecular Devices, Sunnyvale, CA, USA).
One-way ANOVA with repeated measures (RM) design was used to test for significant differences in cardiovascular and ventilatory parameters. Data showing a significant effect, were further analysed by a Fisher's LSD multiple comparison test (P<0.01) to determine at which time periods significant effects were observed.
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Results |
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Ventilation rate (Fig. 1D) increased significantly from between 56-59 beats min-1 to 70 beats min-1 during feeding (F=4.9, P<0.001). These rates were sustained above pre-feeding values for 10 h, before dropping to levels that were not significantly different from those measured pre-feeding (Fisher's LSD test, P<0.001).
There were also significant changes in haemolymph flow rates. Haemolymph flow through the anterior aorta (Fig. 2A), increased 3 h after feeding (F=5.1, P<0.001) and remained elevated for a further 7 h, at which time flow rate decreased to pre-feeding levels. There was an increased perfusion of the hepatopancreas via the hepatic arteries (Fig. 2C): a steady increase in flow rates occurred during feeding, becoming significantly higher than control values 3 h after feeding (F=2.8, P<0.001). Haemolymph flow rates through the hepatic arteries remained elevated for 4 h before decreasing to levels that were not significantly different from those measured pre-feeding. Haemolymph flow through the sternal artery (Fig. 2E) increased substantially from approximately 28 ml min-1 to over 60 ml min-1 during feeding (F=5.8, P<0.001). Thereafter, sternal flow rates decreased to levels that were not significantly different from those measured pre-feeding.
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Despite an apparent increase in flow rates through the anterolateral arteries (Fig. 2B) and the posterior aorta (Fig. 2D) following feeding, no statistically significant change could be demonstrated (F=1.4 and 1.1, respectively, P>0.1).
Feeding followed by hypoxia
Heart rate (Fig. 3A)
increased significantly by approximately 6 beats min-1 during
feeding and remained elevated thereafter (F=8.1,
P<0.001). Once hypoxia was administered there was a steady
decrease in heart rate; after 1 h in hypoxia, heart rate had dropped to
approximately 71 beats min-1, which was 12 beats min-1
lower than rates measured during feeding. On return to normoxia there was
significant increase in heart rate and pre-feeding levels were rapidly
regained. Stroke volume (Fig.
3B) also increased significantly during feeding (F=8.0,
P<0.001), however, this increase was transient and stroke volume
rapidly decreased to pre-feeding levels following administration of food. When
hypoxia was initiated there was a further decrease in stroke volume, dropping
approximately 0.3 ml beat-1 below pre-feeding levels. When the
oxygen tension was restored to normoxic levels, stroke volume increased,
reaching values similar to those measured during pre-feeding. Cardiac output
(Fig. 3C) also increased
transiently during feeding, reaching 91±28 ml min-1 before
dropping back to pre-feeding levels of 62-69 ml min-1. Once hypoxia
was initiated there was a further decrease (F=11.1,
P<0.001) in cardiac output to 40-50 ml min-1; this was
maintained throughout the hypoxic exposure period. As with heart rate and
stroke volume, initiation of normoxia was associated with a rapid but
transient increase in cardiac output; pre-feeding levels were regained within
an hour.
|
Ventilation rate varied between 60 and 63 beats min-1 during control conditions (Fig. 3D). There was a significant increase in rate (F=17.5, P<0.001) to 77 beats min-1 during administration of food. Rates remained significantly elevated thereafter. Upon exposure to hypoxic conditions there was a further significant increase; ventilation rate approached 90 beats min-1. There was a steady decline in rate when normoxic conditions were restored; ventilation rates reached levels that were similar to those measured during the initial feeding phase in normoxia.
There was no significant change in haemolymph flow through the anterior aorta (Fig. 4A) in response to feeding or hypoxia. Haemolymph flow rates through this artery only started to increase significantly (F=3.6, P<0.001) towards the end of the recovery period in normoxia (13-16 h). Although haemolymph flow appeared to increase through the anterolateral arteries (Fig. 4B) during feeding, no statistical significance could be demonstrated (Fisher's LSD test, P>0.05). However, when hypoxia was initiated flow rates decreased below levels measured during both feeding and pre-feeding (F=4.5, P<0.001). When oxygen levels were restored there was a significant increase in flow rates through the anterolateral arteries; control levels were regained within an hour.
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There was no significant change in perfusion of the hepatopancreas, via the hepatic arteries (Fig. 4C), while the crabs were feeding. However, when hypoxia was initiated there was a slight, but significant drop in flow rates (F=2.3, P<0.01). There was no significant change in flows when normoxia was restored (Fishers LSD P>0.05).
There was no significant change in flow rates through the posterior aorta while the crabs were feeding (Fig. 4D). After 2 h in hypoxia, a significant decrease in flow rates occurred (F=3.9, P<0.001). There was an overshoot in flow rates when normoxic conditions were restored; these subsided after 2 h to levels similar to pre-treatment levels.
During feeding, haemolymph flows through the sternal artery (Fig. 4E) increased significantly (F=7.4, P<0.001), before quickly returning to pre-feeding levels. This was followed by a further decrease in haemolymph flow rates during hypoxia. On return to normoxia there was a rapid increase in flow rates, such that during the first hour they increased over pre-feeding levels. Thereafter they decreased to levels that were not significantly different from those measured during pre-feeding.
Hypoxia followed by feeding
A pronounced bradycardia occurred during hypoxic exposure
(Fig. 5A). Heart rate dropped
significantly from between 79-82 beats min-1 to 48-52 beats
min-1. This bradycardia was sustained for the duration of hypoxia
(F=26.9, P<0.001). When the crabs were fed there was a
significant increase in heart rate to 69-72 beats min-1. This was
still significantly lower than heart rates recorded during control conditions.
On return to normoxia there was a further increase and heart rate reached
control levels within an hour. An immediate increase in stroke volume
(Fig. 5B) occurred during
hypoxia, however, this increase was only sustained for 1 h before declining to
control levels (F=5.9, P<0.001). An additional small, but
significant, decrease in stroke volume occurred an hour after feeding; this
rate was sustained until oxygen levels were restored. In normoxia, stroke
volume quickly returned to pre-treatment levels. Changes in cardiac output
(Fig. 5C) were predominately
affected by heart rate. Cardiac output decreased significantly in hypoxia
(F=5.6, P<0.001). When the crabs were fed in hypoxia
there was an increase in cardiac output and pre-treatment levels were
regained. Nevertheless, this increase was not sustained and during the
following 6 h there was a significant decrease in cardiac output, reaching
levels comparable to those measured during pre-feeding in hypoxia. On return
to normoxia there was a significant rise in cardiac output and pre-treatment
levels were rapidly regained.
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Ventilation rates (Fig. 5D) were maintained between mean values of 57-62 beats min-1 during control conditions. There was a rapid increase in ventilation rate when hypoxia was initiated; rates reached over 90 beats min-1 (F=23.6, P<0.001). Although there appeared to be a further increase in rate following administration of food, this proved to be statistically insignificant (Fisher's LSD test, P<0.05). On return to normoxic conditions there was a significant decrease in ventilation rates. However, these rates still remained elevated over pre-treatment levels.
There were also changes in regional haemolymph flow associated with food intake during hypoxia. An immediate increase in haemolymph flow through the anterior aorta (Fig. 6A) occurred when the crabs fed in hypoxia (F=3.0, P<0.001). This increase was only sustained during the feeding phase, after which, flow rates dropped to levels that were not significantly different than pre-feeding values. On return to normoxia there was a slight, transient increase in flow rate through the anterior aorta before returning to pre-treatment levels. A decrease in haemolymph flows through the hepatic arteries (Fig. 6C) occurred when the crabs fed in hypoxia (F=3.6, P<0.001). This decrease was sustained for the duration of the postprandial period in hypoxia. Pre-treatment flow rates were regained within 1 h of transfer to normoxic conditions. Haemolymph flows through the sternal artery (Fig. 6E) exhibited the greatest changes (F=3.7, P<0.001). After 3 h in hypoxia, a slight decrease in flow was apparent. A transient increase in flow rates occurred during feeding before dropping back to levels that were not significantly different to those measured pre-treatment. On return to normoxia, pre-treatment levels were rapidly regained.
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Despite apparent changes in flow rates through the anterolateral arteries (Fig. 6B) and the posterior aorta (Fig. 6D) no statistically significant difference could be demonstrated in either case (F=0.9 and F=1.4, respectively, P>0.1).
L-Lactate levels
Haemolymph lactate levels varied between 0.56 and 1.12 mmol l-1
in starved crabs (Fig. 3D) in
normoxia (Table 1A,B). When
crabs were fed in normoxia (Table
1A) there was no significant change in lactate levels. After 6 h
exposure to hypoxic conditions, there was a statistically significant rise in
haemolymph lactate, reaching 1.22±0.21 mmol l-1
(F=4.71, P<0.01). When normoxic conditions were restored,
haemolymph lactate levels dropped to pre-feeding values
(Table 1A).
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After 3 h exposure to hypoxia, lactate levels increased slightly (Table 1B), but these levels were not significantly higher than those measured during normoxia (Fisher's LSD test, P>0.01). There was no significant change in lactate levels 6 h after feeding in hypoxia (Fisher's LSD test, P>0.01). When normoxic conditions were restored, lactate levels dropped to 0.56±0.12. These were significantly lower than those measured after 3 h exposure to hypoxia (F=5.54, P<0.01).
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Discussion |
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Cardiac and ventilatory parameters increased immediately in Cancer
magister following feeding. These responses were a direct action of food
on metabolism, since administration of an equal amount of saline caused only
slight and transient increases (not shown). The immediate increase in cardiac
and ventilatory parameters were associated with food handling and food
processing in the foregut (Carefoot,
1990). Following this initial increase, cardiac and ventilatory
parameters remained elevated for up to 10 h, reflecting their involvement in
protein synthesis (Houlihan et al.,
1990
; Mente, 2003
;
Mente et al., 2003
). A
standardised amount of food was delivered to each crab to reduce variation
associated with meal size (Mente,
2003
) and to synchronise feeding time. This feeding method also
aimed to reduce some of the activity associated with feeding (apparent
specific dynamic action; Carefoot,
1990
). Nevertheless, the crabs still moved the mouthparts and
chelae when food was administered: this was seen as an increase in flow
through the sternal artery (Fig.
2E), which supplies these structures
(McGaw, 2005
). Haemolymph flow
rates through the hepatic artery (which supplies the hepatopancreas) increased
3 h after feeding, which corresponds closely with the time that protein
synthesis increases in the hepatopancreas
(Houlihan et al., 1990
).
The magnitude of changes in heart rate during hypoxia
(Fig. 5A) were similar to those
reported previously for unfed Cancer magister
(Airriess and McMahon, 1994).
However, these researchers reported the bradycardia was associated with a
sustained increase in stroke volume, resulting in maintained cardiac output.
In the present study the increase in stroke volume was only transient and not
large enough to affect cardiac output (Fig.
5B,C). This difference may have arisen because of differences in
experimental design. Previous experiments were performed on restrained animals
(McMahon and Wilkens, 1975
;
Reiber, 1995
;
Reiber and McMahon, 1998
) or
in chambers that allowed minimal movement
(Wilkes and McMahon, 1982
;
Airriess and McMahon, 1994
).
When crabs are restrained during such experiments they will continue to
struggle (personal observation). The untethered approach used in this study
reduces stress associated with instrumentation
(McDonald et al., 1977
;
Hassall and McMahon, 1980
) and
the layer of sand in the tank minimizes sensory stimulation to the crabs
(Florey and Kriebel, 1974
).
These assertions are upheld by observations that heart rates recorded in
situ, in the natural environment, may differ from responses observed in
the lab (Styrishave et al.,
2003
). The changes in stroke volume and cardiac output in the
present study (Fig. 5B,C) are
also emulated by behavioural observations: Cancer magister was active
during the initial oxygen reduction period, but became quiescent, exhibiting
little or no movement thereafter. The crabs remained inactive until oxygen
levels dropped to 1.5 kPa, but below these levels they became agitated and
attempted to escape (J. L. Bernatis and I.J.M., unpublished observation).
Therefore, the data obtained in the present study may be the result of
behavioural differences associated with experimental design.
Food intake during hypoxia clearly affected heart rate, reducing but not
abolishing, the bradycardic response. Therefore, in the case of heart rate,
addivity of effects occurs, rather than prioritization of one or other of the
systems (Bennett and Hicks,
2001). Because the bradycardic response was reduced by feeding,
its physiological role may be diminished. Increased mortality occurs in the
shore crab Carcinus maenas when sufficient oxygen cannot be supplied
following feeding in hypoxia (Legeay and
Massabuau, 2000b
). However, both starved and postprandial
Cancer magister survived 48 h exposure to 2.1 kPa water (unpublished
observation). This suggests that although bradycardia may aid survival of
Cancer magister in low oxygen environments
(Airriess and McMahon, 1994
),
its role is only minor and other compensatory mechanisms are involved.
Although, both heart and ventilation rates showed addivity as a result of
the effects of hypoxia and food intake, blood flow events tended to be
prioritized. Following a transient increase in haemolymph flow rates to the
mouthparts, via the sternal artery and anterolateral arteries (Figs
4B,E,
6B,E) there was a trend towards
a decrease in arterial flow rates. The anterior aorta was the only artery in
which flow was maintained (Figs
4A,
6A). This artery supplies the
supraoesophageal ganglion of the crab
(McGaw and Reiber, 2002;
McGaw, 2005
) so it is
important to maintain a blood supply to this organ. The general decrease in
haemolymph flow is the opposite to the pattern occurring in feeding alone
(Fig. 2); thus digestion must
be slowed, prioritizing blood flow for other processes. This assertion is
substantiated by an overall decrease in whole animal protein synthesis in
shore crabs in 3 kPa hypoxia (Mente,
2003
; Mente et al.,
2003
). Since protein synthesis is an energetically costly process,
accounting for over 50% of oxygen uptake, then a decrease in protein synthesis
may be vital to the reduction of a hypoxic crabs energy budget
(Mente, 2003
). Most notably
during hypoxia, a steady decline in protein synthesis occurs in hepatopancreas
2 h after feeding (Mente,
2003
). This time period correlates closely with decreased blood
flow to this organ (Figs 4C,
6C). There was also a
concomitant decrease in flow through the anterolateral arteries
(Fig. 4B), which supply the
foregut region. Decreasing oxygen levels modulate foregut contraction causing
uncoupling of gastric and pyloric rhythms and a slowing of food filtering in
the pyloric stomach (Massabuau and
Meyrand, 1996
; Clemens et al.,
1998
). This response is opposite to the sea bass Dicentrarchus
labrax, which maintain gut blood flow during hypoxia and is thus
committed to digestion following feeding
(Axelsson et al., 2002
). It
appears that Cancer magister can delay digestion after feeding,
sparing oxygen for other systems.
In contrast to the present observations, Legeay and Massabuau
(1999) reported a
calculated increase in blood flow (measured using the Fick
principle), facilitating oxygen delivery in postprandial Carcinus
maenas in hypoxia. Measurement of blood flow using the Fick principle
involves disturbing the animal and does not record instantaneous changes in
flow (Airriess and McMahon,
1994
). Pulsed-Doppler measurements used here have an advantage,
they allow second by second changes to be monitored in untethered, undisturbed
animals (Airriess et al.,
1994
). In the Dungeness crab, since haemolymph flows (and hence
cardiac output) decreased after the crabs fed
(Fig. 4B-E), alterations in
cardiac output cannot account for increased oxygen delivery. The benefit of
decreased cardiac output would be a higher haemolymph residence time in the
gills, coupled with an increased ventilation rate (Figs
3D,
5D) this could allow a higher
saturation of the branchial excurrent haemolymph, as well as an increased
oxygen extraction from the circulating haemolymph
(Larimer, 1964
). Other
mechanisms could be used to compensate for changes in cardiac parameters.
Ventilation rates showed additivity of effects, increasing in response to both
food intake and hypoxia, which would help in extra oxygen delivery. In
addition to physiological changes, internal compensatory mechanisms will take
over (McMahon, 2001
). Changes
in acid-base balance can enhance oxygen carrying capacity of the haemolymph
(Legeay and Massabuau, 1999
).
Oxygen binding affinity of haemocyanin can also be enhanced by increasing
lactic acid levels, such as those occurring during mild anaerobic metabolism
(Truchot, 1980
).
Cardiac and ventilatory parameters rapidly returned to control levels when
normoxic conditions were restored. Since no overshoot in physiological
parameters was observed, this suggests no oxygen debt was incurred during the
hypoxic period (Herried,
1980). The low level of L-lactate production during
experiments (Table 1) also
indicates anaerobic respiration was negligible. For comparison, during
strenuous walking activity, lactate levels in Cancer magister
increase from 0.7 mmol l-1 up to 11.1 mmol l-1
(McDonald et al., 1979
). The
L-lactate levels for Cancer magister are much lower than
those reported for postprandial green crabs, Carcinus maenas, in
similar hypoxic conditions (Mente et al.,
2003
). This suggests that Cancer magister is more
tolerant of hypoxia than Carcinus maenas: Cancer magister is
commonly found in muddy bays where dissolved oxygen levels drop below 1 kPa
(Bernatis and McGaw, unpublished observation), whereas Carcinus
maenas typically inhabits rocky shorelines. Indeed the
Pcrit for Cancer magister lies below 1.3 kPa
(I.J.M. and J. L. Bernatis, unpublished observation).
In some instances behavioural regulation may be employed by crustaceans as
a means of avoiding hypoxia, thus negating the use of physiologically costly
processes (Taylor and Spicer,
1988). For example, in the laboratory, postprandial Dungeness
crabs will select higher oxygen regimes to digest food
(Bernatis and McGaw, 2004
).
However, in Barkley Sound, areas of widespread hypoxia are common and
behavioural avoidance of such areas may not be possible
(Bell et al., 2003
), therefore
physiological mechanisms will be used.
The present study has shown the nutritional status of an animal can alter physiological mechanisms. Consequently, `controlled' laboratory experiments, where animals are starved prior to experimentation, may not be wholly representative of physiological processes in the natural environment. This underscores the importance of an integrative approach, studying physiological responses at the organismal level.
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Acknowledgments |
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