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First published online September 19, 2006
Journal of Experimental Biology 209, 3777-3785 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02442
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Feeding and digestion in low salinity in an osmoconforming crab, Cancer gracilis II. Gastric evacuation and motility
School of Life Sciences, University of Nevada, Las Vegas, NV 89154-4004, USA and Bamfield Marine Sciences Centre, Bamfield, British Columbia, VOR 1BO, Canada
e-mail: iain.mcgaw{at}unlv.edu
Accepted 12 July 2006
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: Cancer gracilis, crab, digestion, gastric evacuation, feed, salinity
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Barker and Gibson, 1978;
Icely and Nott, 1992;
Heeren and Mitchell, 1997).
The cardiac chamber contains calcified ossicles, which form the gastric mill
apparatus (Maynard and Dando,
1974). Its primary function is mastication of food
(Heinzel, 1988;
Heinzel et al., 1993);
enzymatic breakdown of food also starts in this region
(Icely and Nott, 1992). The
pyloric chamber acts to regulate movement of material into the midgut region.
The midgut starts at the junction with the pyloric sac and ends in a coiled
tube, the posterior midgut caecum, at the junction between the carapace and
abdomen (Smith, 1978). The
paired anterior midgut caeca arise from the midgut close to the junction with
the pyloric chamber and branch extensively within the hepatopancreas. It is
here that enzymatic digestion continues and absorption of food by the
hepatopancreas occurs (Hopkin and Nott,
1980). The hindgut arises behind the posterior midgut caecum and
runs the length of the abdomen to the anus
(Maynard and Dando, 1974). It
functions in expelling the muco-peritrophic membrane and its contents by
rhythmic contractions along its length
(Dall and Moriarity,
1983).
The duration of food passage through the gut is variable among different
species of decapod crustaceans, ranging from as little as 3-6 h to as long as
48 h (Haddon and Wear, 1987;
Hill, 1976;
Hopkin and Nott, 1980;
Joll, 1982;
Sarda and Valadares, 1990;
McGaw and Reiber, 2000).
Release of enzymes from the hepatopancreas and subsequent digestion occurs
within 30-60 min of food ingestion (Dall,
1967; Barker and Gibson,
1977; Barker and Gibson,
1978; Hopkin and Nott,
1980) and intracellular digestion and protein synthesis can start
within 2 h and continue for 2-3 days
(Houlihan et al., 1990;
Mente, 2003;
Mente et al., 2003). The whole
system is cleared of food between 12 h and 48 h after feeding
(Dall, 1967; Hopkins and Nott,
1980; Joll, 1982;
Choy, 1986;
Sarda and Valladares, 1990).
Movement of material through the digestive system is highly dependent on
temperature (Haddon and Wear,
1987). In addition, gastric rhythms are modulated by hypoxia
(Clemens et al., 1998a) and low
salinity slows egestion rates in mysid shrimps
(Roast et al., 2000).
Otherwise there are few other reports of environmental effects on gastric
processing in crustaceans.
Feeding and digestion and the subsequent assimilation of nutrients causes
an increase in metabolic parameters, a process known as specific dynamic
action. This is due to food handling and mechanical breakdown in the gut
(Carefoot, 1990), and the
subsequent intracellular protein synthesis
(Houlihan et al., 1990;
Mente, 2003). In crustaceans
the specific dynamic action is associated with a two- to threefold increase in
oxygen uptake that persists for up to 3 days
(Houlihan et al., 1990;
Burggren et al., 1993;
McGaw and Reiber, 2000;
Robertson et al., 2002;
McGaw, 2006b). To support the
increase in metabolic rate and to facilitate the uptake and distribution of
absorbed nutrients, changes in cardiac function and haemolymph distribution
also occur during the digestive process
(McGaw and Reiber, 2000,
McGaw, 2005;
McGaw, 2006a;
McGaw, 2006b).
There is a growing body of literature on the cardiovascular and respiratory
responses of decapod crustaceans to low salinity (see
McGaw, 2006b). However, these
previous studies were conducted on unfed animals to ensure they were in a
similar metabolic state and to avoid stimulatory effects associated with
feeding and digestion (Wang,
2001). Recent work on decapod crustaceans shows that digestion can
pose additional demands on physiological systems, leading to an increased
mortality rate of postprandial crabs in low salinity
(Legeay and Massabuau, 2000;
McGaw, 2006a). Therefore, the
ability of an animal to balance the demands of physiological systems by either
prioritizing or summing metabolic effects is important
(Bennett and Hicks, 2001).
The graceful crab Cancer gracilis is classed as an osmoconformer
and does not survive prolonged exposure below 55%SW (D. L. Curtis, E. K.
Jensen and I. J. McGaw, manuscript submitted for publication). In contrast to
work on unfed osmoregulating crabs, which exhibit an increase in oxygen uptake
and heart rate during low salinity exposure
(King, 1965;
Engel et al., 1975;
Hume and Berlind, 1976;
Taylor, 1977;
McGaw and McMahon, 1996;
McGaw and Reiber, 1998), unfed
Cancer gracilis react with a pronounced decrease in cardiac and
respiratory parameters. However, when postprandial Cancer gracilis
encounter low salinity, the bradycardia is absent and the reduction in oxygen
uptake is of shorter duration than in unfed crabs
(McGaw, 2006b). This suggests
that either digestive events are prioritized and digestion continues unabated
in low salinity or, because of the elevated metabolism due to the specific
dynamic action, increases in respiratory and cardiovascular parameters are
necessary to sustain basic life functions. Since digestive events can pose an
additional burden on an already taxed system
(Legeay and Massabuau, 2000;
McGaw, 2006a;
McGaw, 2006b) the ability to
alter or delay digestion may be an advantage. Therefore, the present study
sought to determine how gastric processing and evacuation are affected or
modulated by exposure to low salinity in an osmoconforming species of
crab.
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Materials and methods |
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at 11±1°C)
for a week prior to experimentation. Crabs were fed fish every other day, but
were isolated from the general population and starved for 3 days prior to
experimentation. This time period allowed all food to be evacuated from the
digestive system, but avoided large-scale physiological changes associated
with starvation (Wallace,
1973).
During experiments the crabs were housed in individual chambers of 0.2
mx0.2 m. They were allowed to settle for 12 h in the chambers before
experimentation. All experiments were performed in constant light, which
helped standardize activity levels, and the tanks were surrounded by black
plastic to avoid visual disturbance to the animals. The crabs were fed a
radioopaque meal consisting of the following by mass: 65% liquefied fish
muscle (Sebastes species), 25% gelatin solution and 10% electrolytic
iron powder. This produced a homogenous solid food that could be cut into
cubes and was readily consumed by the crabs. Electrolytic iron powder was a
better tracer than barium sulphate, which had to be used in such a high
concentration that it made the meal unpalatable
(Talbot and Higgins, 1983) and
ballotini lead glass beads are no longer commercially available. In the first
set of experiments, passage of the particulate digesta through the digestive
system and contraction of the foregut was followed in 100%SW, 80%SW and 60%SW
(N=10 per salinity). These salinities were chosen because they were
within the survivable range for this species (D. L. Curtis, E. K. Jensen and
I. J. McGaw, manuscript submitted for publication). The crabs were offered 5 g
cubes of food (approx. 2% of body mass) in 100%SW (32). Once they had
finished feeding (approx. 15 min), the salinity was lowered by draining a
portion of tank, without aerially exposing the crab, and adding a known volume
of freshwater at ambient temperature and oxygen levels. Salinity was checked
using a YSI 30 conductivity meter (Yellow Springs, OH, USA). New steady states
of salinity were reached within 10 min and did not vary by more than
0.1 during experiments. In a second experiment, food passage was
followed during a salinity cycle, representative of those experienced in the
field (McGaw, 2006b). The
crabs (N=10) were fed in 100%SW and allowed to digest for 3 h in
100%SW. The salinity was then lowered to 65%SW for 6 h, before being raised
back up to 100%SW.
For X-ray analysis, a plastic box (120 mmx180 mmx 80 mm) was
submerged in the chamber and the crabs were coaxed into the box and allowed to
settle for 30 s. The box was then placed under a LIXI PS500 OS X-ray system
(Huntley, IL, USA) and images were recording using LIXI image processing
software. Technical specifications for the X-ray were 35 kV tube voltage, 155
µA tube current with a 5 cm focal window. At hourly intervals following
feeding a still image and 15 s segment of video were captured. The passage of
food through the gut was measured by outlining the boundaries of each gut
region and estimating the percentage fullness of each region, separately. The
movement of the digesta and marker were followed until the latter had been
voided in the faeces and the time of emptying of the foregut, midgut and
hindgut regions was calculated (Edwards,
1971; McGaw and Reiber,
2000). Contraction rates of the cardiac region and pyloric region
of the foregut were also recorded (Fig.
1). Cardiac movements were counted as opening and closing of the
gastric mill and contraction and squeezing of the cardiac stomach
(Heinzel, 1988). Contractions
of the pyloric region were counted as small-scale pulsating movements
(Heinzel, 1988). Only crabs
that appeared to have a full stomach after feeding were used in analysis.
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Repeated-measures ANOVAs were used to test for significant differences in gut parameters. Data showing a significant effect, were further analyzed 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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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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There were also significant differences in evacuation of the hindgut as a function of salinity (ANOVA, F=7.86, P=0.001). Digesta did not appear in the hindgut in significant amounts until 6 h in 100%SW, 8 h in 80%SW and 11 h in 60%SW. In 100%SW the digesta moved relatively slowly through the hindgut, reaching maximal levels at 18 h and declining slowly thereafter. The hindgut was cleared between 48 h and 72 h (Fig. 2A). In 80%SW less digesta was apparent in the hindgut. Maximal levels were reached at 24 h and digesta was still evident in the hindgut at 72 h. In contrast in 60%SW only a small amount of digesta entered the hindgut. Levels started to rise after 12 h and continued to increase up to 72 h. The mean time of emptying of the hindgut was 96±4 h (Fig. 5) although in some cases digesta was still visible at 108 h.
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Mean emptying times of each area of the gut are shown in Fig. 5. There was a dose dependent increase in time of foregut emptying as a function of salinity (ANOVA, F=17.01, P<0.001). The mean time for foregut emptying in 100%SW was 9.4±0.65 h, which was significantly faster than times measured during exposure to both 80%SW and 60%SW (Fisher's LSD, P<0.01). During exposure to 80%SW the foregut was cleared at 23±3.73 h, which was significantly faster than the 47.89±8.08 h recorded in 60%SW (Fisher's LSD, P<0.05). There was a similar pattern in emptying times of the midgut (ANOVA, F=28.89, P<0.001). In 100%SW the midgut was cleared after 21.4±2.7 h, which was significantly faster than times measured in 80%SW and 60%SW. Midgut emptying times of 45.6±3.48 h were significantly faster than the 72.67±8.4 h recorded in 60%SW (Fisher's LSD, P<0.001). In 100%SW Cancer gracilis cleared the entire system after 49.2±2.8 h, which was significantly faster than gut emptying times recorded in 80%SW and 60%SW (ANOVA, F=32.01, P<0.001). Gut emptying times of 84.1±5.34 h in 80%SW and 96±4 h in 60%SW were not significantly different from one another (Fisher's LSD, P>0.05).
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In 100%SW food started to move into the midgut after 2 h (Fig. 7A; ANOVA, F=8.68, P<0.001) and the midgut was 50±7.76% full when 65%SW was initiated. There was no further significant change in the percentage of food within midgut region during low salinity exposure (Fisher's LSD, P>0.01); at 9 h the midgut was still 38.5±5.87% full. The midgut emptied slowly on return to 100%SW and after 3 h in 100%SW the percentage of food within the midgut had dropped below pre-treatment levels.
Entry of digesta and marker into the hindgut region was routinely slow; only a small amount of digesta (6.6±2.1%) had entered the hindgut when low salinity was initiated. There was no further significant change in hindgut filling during low salinity exposure. Movement of digesta into the hindgut remained slow when 100%SW was reinstated. Hindgut filling only increased significantly (ANOVA, F=12.07, P<0.001) to 11.17±3.5% after 5 h in 100%SW.
In 100%SW the number of cardiac gut contractions ranged between 5 and 8 min-1 (Fig. 7B). Towards the end of the time period in 65%SW (8-9 h), the number of contractions reached 19±13 min-1. Theses were higher than levels recorded during 100%SW and during the first few hours of low salinity exposure (Fig. 7B; ANOVA, F=2.77, P<0.01). After 2 h recovery in 100%SW levels had dropped to pre-treatment rates (Fig. 5B). There were also significant changes in pyloric gut contractions (Fig. 7B; ANOVA, F=8.04, P<0.001). There was a sharp drop in contraction rates in the first 3 h in 100%SW, from 86.4±9.1 to 52.4±4.1 min-1. Apart from a slight decrease during the first hour of low salinity exposure, there was no further change in contraction rates until 8 h. At this time contraction rate had dropped below pre-treatment levels. On return to 100%SW there was a slow increase in contraction rates. Pre-treatment rates started to be regained after 3 h recovery in 100%SW.
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Discussion |
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; Bucking and Wood,
2006). Electrolytic iron powder has been used with success to
measure food intake and gastric evacuation in fish. It is easily incorporated
into feed in relatively low concentrations, it is not absorbed across the
epithelium of digestive tract (Talbot and
Higgins, 1983) and it is readily eaten by the crabs. Addition of
electrolytic iron appeared to have no effect on time for food passage; the
first faeces appeared at similar times to iron-free food. Barium sulphate was
found to be an unsuitable marker because it had to be used in such high
concentrations that it made the meal unpalatable
(Edwards, 1971;
Jobling et al., 1995).
Ballotini lead glass beads have been used previously to measure food uptake in
lobsters (Thomas et al.,
2002). However, crabs can sort large particles in the pyloric
setae (Dall, 1967;
Smith, 1978) (I. D. McCarthy,
personal communication). This sorting did not occur with the iron powder. The
only drawback was that individual particles could not be counted in order to
quantify food intake (Talbot and Higgins,
1983; Thomas et al.,
2002). This was not a problem, however, since the present study
investigated gut contraction rate and gastric evacuation, and not actual
intake levels.
Food appeared in the stomach as soon as the animals had fed. Only crabs
with stomachs that appeared full were used in the analysis to avoid any
inconsistencies associated with meal size
(Clemens et al., 1998b;
Bernard and Doreau, 2000). In
100%SW seawater, food started to move into the midgut region within 2 h.
Similar processing times have been reported for Metapenaeus bennettae
(Dall, 1967), Scylla
serrata (Hill, 1976) and
Callinectes sapidus (McGaw and
Reiber, 2000). The finger-like midgut caeca did not appear in the
radiographs. Inert material is not found in this region because it is filtered
out at the entrance of the midgut caeca ducts and only liquid and particles
less than 100 nm in diameter enter the hepatopancreas
(Smith, 1978;
Hopkin and Nott, 1980). The
particulate digesta continued its path along the midgut and reached the
hindgut after approximately 6-7 h. This is comparable to the rate measured for
Callinectes sapidus (McGaw and
Reiber, 2000). The foregut was emptied at around 9 h, again this
is comparable to similar sized Callinectes sapidus
(McGaw and Reiber, 2000). The
gut system was completely emptied after 49 h. This is somewhat longer than
times reported for other species (Dall,
1967; Barker and Gibson,
1978; Joll, 1982;
Sarda and Valladares, 1990;
McGaw and Reiber, 2000).
However, this time period took into account a small amount of digesta that
remained in the posterior part of the hindgut. This also occurs in
Carcinus maenas, and this digesta may not even be voided until a
subsequent meal is ingested (Hopkin and
Nott, 1980).
Postprandial Cancer gracilis exhibit different cardiovascular and
respiratory responses to low salinity, compared with unfed individuals
(McGaw, 2006b). Instead of a
decrease in ventilatory and cardiac function, the levels remain unchanged or
even increase (McGaw, 2006b).
Thus, there is a prioritization of cardiac and ventilatory responses to
digestion, suggesting that food processing is continuing unabated
(McGaw, 2006b). However, the
results of the present study refute this assumption. Salinity slowed digestive
processes and increased the time for gastric evacuation
(Fig. 2). Although the crabs
could slow digestive processes, they could not halt it completely: the
particulate digesta eventually moved into the midgut, and presumably the
liquid phase would then enter the midgut caeca where digestion would take
place (Icely and Nott, 1980). Once intracellular digestion begins the crabs
may be committed to it and have to adjust their physiological responses
accordingly (Houlihan et al.,
1990; Mente, 2003;
Mente et al., 2003). Thus,
changes in cardiac and respiratory parameters in postprandial crabs in low
salinity probably function to maintain efficient oxygen delivery associated
with the increased postprandial metabolism, rather than to support mechanical
digestion.
Two types of movements of the cardiac stomach have been described
(Heinzel, 1988): chewing and
grinding by the gastric mill, and contraction or `squeezing' by the stomach
muscles. In the present study these movements were not differentiated.
Movements of the cardiac region of the foregut were sporadic and were not
observed in every animal. This sporadic pattern of contraction is also
reported for Homarus americanus
(Morris and Maynard, 1970),
Cancer magister, Cancer productus
(Powers, 1973), Panulirus
interruptus (Heinzel,
1988) and Cancer pagurus
(Heinzel et al., 1993).
Because movements were sporadic and the crabs were only observed under the
fluoroscope for about 60 s at a time, this probably accounted for the lack of
a discernible pattern of cardiac stomach activity in low salinity
(Fig. 6A). The foregut was
usually emptied within 12 h. However, contractions of the empty stomach were
still evident; this has been reported previously, and it functions for mixing
and pumping of digesta through the midgut
(Clemens et al., 1998a).
Pyloric contractions of the gut regulate movement of the food into the midgut
(Heinzel, 1988). In the X-ray
preparations these were seen as small amplitude `pumping' type contractions.
The contractions were more stable and rapid than those of the cardiac region;
rates of 60-85 min-1 agree with data for other species
(Morris and Maynard, 1970;
Powers, 1973;
Heinzel, 1988;
Heinzel et al., 1993). Pyloric
contractions varied with both time and salinity. Contraction rates decreased
significantly, 2 h after feeding (Fig.
6B). A rapid processing of food during the first hour after
feeding, followed by a decrease in pyloric contractions, are also reported for
Homarus americanus (Morris and
Maynard, 1970) and Jasus lalandii
(Rezer and Moulins, 1983). In
60%SW contraction rates were lower than those measured in 100%SW and 80%SW.
This decrease in foregut processing, coupled with regurgitation of food
(Fig. 4), resulted in
significantly less food being moved into the midgut
(Fig. 2C). It is known that the
stomatogastric ganglion, which innervates the foregut, can be modulated by
exogenous sources (Powers,
1973). These include the presence of food material
(Powers, 1973;
Rezer and Moulins, 1983;
Clemens et al., 1998b),
internal oxygen levels (Massabuau and
Meyrand, 1996; Clemens et al.,
1998a) and a variety of neurohormones
(Weimann, 1992;
Heinzel et al., 1993). Other
than these, there are very few reports on modulation of mechanical digestion
in crustaceans. The results from the present study now add low salinity as a
possible modulator of the stomatogastric ganglion.
Exposure to 60%SW, which is just above what is considered a survivable
salinity for this species (55%SW) (D. L. Curtis, E. K. Jensen and I. J. McGaw,
manuscript submitted for publication), induced a vomiting response. Rapid
contractions of the gastric mill and cardiac stomach muscles expelled food out
through the oesophagus. This occurred between 6 h and 12 h after feeding. The
exact function is unclear, but in animals that regurgitated food, very little
was processed in the midgut. It could be a `protective response', preventing
digestion of the food and subsequent metabolic increases associated with
protein synthesis. Alternatively, it could be a simple stress response to low
salinity exposure. To argue against the latter, a stress response might be
expected to occur more rapidly, because crabs exhibit the greatest changes in
activity (McGaw et al., 1999)
(D. L. Curtis, E. K. Jensen and I. J. McGaw, manuscript submitted for
publication) and cardiovascular and respiratory responses
(McGaw and McMahon, 1996;
McGaw and Reiber, 1998;
McGaw, 2006a;
McGaw, 2006b) within the first
hour or two of low salinity exposure. Clearly further investigation on
alterations in enzyme activity and protein synthesis, before and after
regurgitation, needs to be carried out before definite conclusions can be
drawn.
Following the digestive processes during a salinity cycle allowed changes
in gastric processing to be differentiated more clearly
(Fig. 7). An increase in
foregut contraction rate occurred towards the end of the low salinity period.
This increase in contraction did not move more food into the midgut
(Fig. 7A); rather it was
associated with vomiting the stomach contents. A rapid overshoot in cardiac
and ventilatory parameters occurs when 100%SW is restored
(McGaw, 2006b). Because gut
processing and movement of digesta through the gut was only regained slowly
upon return to 100%SW this overshoot in cardiac and respiratory physiology is
likely to pay off an oxygen debt incurred during low salinity, because low
salinity increases haemocyanin oxygen binding affinity [in Carcinus
maenas (Truchot, 1973)]
just at a time when extra oxygen is needed for protein synthesis.
In Cancer gracilis low salinity had a dose-dependent effect on gut
processing, increasing the time for gastric evacuation and reducing the amount
of food processed. It is unclear whether this is an active `decision' to
reduce the specific dynamic effect by processing less food
(Wang et al., 1995) thus
sparing energy for other systems or, because of the physiological demands
associated with hyposaline exposure, there are simply not enough resources to
be diverted to digestion. Future studies involving measurement of gastric
processing and evacuation in weakly regulating and strongly regulating species
are planned to compare and contrast with those of the osmoconformer Cancer
gracilis. This will allow us to determine whether stronger regulators are
able to balance the demands of physiologically competing systems.
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Acknowledgments |
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References |
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