L
Journal of Experimental Marine Biology and Ecology, 241 (1999) 179–192
Developmental changes in oxygen uptake in Cancer magister
(Dana) in response to changes in salinity and temperature
*
A. Christine Brown , Nora B. Terwilliger
Oregon Institute of Marine Biology, University of Oregon, Charleston, OR 97420, USA and Department of
Biology, University of Oregon, Eugene, OR 97403, USA
Received 5 August 1998; received in revised form 10 May 1999; accepted 15 May 1999
Abstract
The various life stages of the Dungeness crab, Cancer magister, may experience broad environmental fluctuations in both salinity and temperature, parameters that can affect nearly all aspects of their physiological function. The routine rates of oxygen uptake of megalopa, first and fifth instar juvenile and adult C. magister were measured, using closed vessel respirometry over 8 h during acute exposure to 100, 75 and 50% seawater at 10 and 208C. At 108C there is no significant effect of salinity on the rate of oxygen uptake of the megalopa. At 208C, however, the rate of oxygen uptake rises and is greater at 75 and 50% SW than in 100% SW. The rates of oxygen uptake of the first instar juvenile, fifth instar juvenile and adult are not affected by salinity at either 10 or 208C. The oxygen uptake of the fifth instar juvenile is less temperature sensitive, at all salinities, than the other stages examined. Weight specific cardiac output is affected by both salinity and temperature. The effect of temperature on cardiac output is especially pronounced for the first instar juvenile. The first instar juvenile is the first benthic stage and therefore is an important step in recruitment of crabs in the estuary. The differences in metabolic response between the stages indicate that the first instar juvenile, in particular, may be very near the limit of its respiratory and circulatory capacities as a result of tidal changes in salinity and temperature in the intertidal estuarine habitat. 1999 Elsevier Science B.V. All rights reserved.
Keywords: Cancer magister; Cardiac output; Crustacean development; Oxygen uptake; Salinity; Temperature
*Corresponding author. Correspondence address: Department of Life Sciences, University of New England, 11 Hills Beach Rd., Biddeford, ME 04005, USA. Tel.: 11-207-283-0171.
E-mail address: [email protected] (A.C. Brown)
1. Introduction
The Dungeness crab, Cancer magister, goes through a complex combination of morphological, physiological, and distributional changes during development. The larval stages are planktonic and are found up to and beyond 150 km offshore (Lough, 1976; Hobbs et al., 1992), while metamorphosis from megalopa to juvenile, and recruitment of juveniles occurs in coastal and estuarine waters. The young of the year juvenile crabs can be found in large numbers on the intertidal mudflats in the Coos River estuary (438
219N, 1248189W) throughout their first summer. Adult C. magister occur primarily in deeper estuarine and nearshore waters. The maximum dredged depth of the Coos River is about 14 m at the entrance. Despite their different distributions and utilization of different habitats, estuarine megalopas, juveniles and adults are exposed to regimes of changing environmental salinity and temperature due to the tides.
These types of changes in salinity and temperature, essentially acute exposure for the 6–8 h of a tidal cycle, typically cause changes in the aerobic metabolism of crustaceans. There are data available on metabolic response to salinity and / or temperature for adults of many species of decapod crustaceans. These include Hemigrapsus nudus and
Hemigrapsus oregonensis (Dehnel, 1960), Panopeus herbstii (Dimock and Groves,
1975), Carcinus maenas (Taylor, 1977), Callinectes sapidus (Findley et al., 1978), and
Ilyoplax gangetica (Savant and Amte, 1995). This topic has also been reviewed by
Scholander et al., 1953; Kinne, 1964; Vernberg, 1983 and Morris, 1991.
Data on the effects of salinity and / or temperature on the oxygen consumption rates of early life stages of decapod crustaceans are also available, including studies on Uca spp. (Vernberg and Costlow, 1966), Callinectes sapidus (Leffler, 1972), Carcinus maenas (Klein Breteler, 1975), Cancer magister (Gutermuth and Armstrong, 1989), and
Callinectes similis (Guerin and Stickle, 1997). The temperature and salinity sensitivity
of metabolic rates of different developmental stages may vary greatly. Changes in sensitivity to temperature and salinity between the life stages in a given species tend to correspond to such ecological factors as changes in habitat utilization or seasonal shifts in environmental salinity and / or temperature.
An important developmental change in C. magister is the stage specific difference in ionic regulation (Brown and Terwilliger, 1992). In megalopas first and fifth instar juveniles and adults of C. magister exposed to 50, 75 and 100% seawater (SW) at 10 and 208C, all stages can be characterized as weak hyperosmoregulators. However, the hemolymph magnesium concentrations in megalopas and juveniles acclimated to 100% SW were twice that of the adults. After 8 h exposure to 50% SW the adults had maintained constant hemolymph magnesium levels, while the hemolymph magnesium levels in the megalopas and juveniles had decreased to the same level as the adult hemolymph magnesium concentration. Hemolymph calcium ion is regulated by both megalopas and adults in all salinity exposures. On the other hand, hemolymph calcium is much less well regulated in the juvenile stages.
lacks subunit six, which is present in the adult (Terwilliger and Terwilliger, 1982). Functionally, the intrinsic oxygen affinity of the larval / juvenile 25S hemocyanin is half the oxygen affinity of the adult 25S hemocyanin under identical experimental conditions (Terwilliger et al. 1986). The oxygen affinities of the stage specific 25S hemocyanins show differential sensitivity to the effects of calcium and magnesium ion concentrations (Terwilliger and Brown, 1993). In the whole hemolymph of animals from 100% SW and normal temperatures (¯108C), however, the apparent oxygen affinity is indistinguish-able between the stages (Brown and Terwilliger, 1998), due at least in part to differences in hemolymph ion concentrations.
All of these factors, developmental stage, habitat, ionic and osmotic regulatory patterns, and hemocyanin oxygen transport function, will affect the overall metabolism of an animal exposed to changes in salinity and temperature. Measurement of oxygen uptake, as an estimate of metabolism of an organism, assuming aerobic metabolism, is a valid method of assessing the organismal response to changes in the environment (Cameron, 1989). In order to determine the extent of physiological stress that a certain combination of external parameters imposes on an organism it is useful to look at oxygen uptake and some of the functional features of the respiratory protein in oxygen transport. This study examines oxygen uptake of four life stages of C. magister exposed to various salinities and temperatures that were determined to mimic the habitat changes experienced by the life stages due to semidiurnal tides. The results are discussed in conjunction with C. magister hemocyanin oxygen dissociation properties (Terwilliger and Brown, 1993; Brown and Terwilliger, 1998) and blood gas parameters (Johansen et al., 1970). Estimated cardiac output necessary to fuel the apparent oxygen uptake is also discussed as a measure of performance of the circulatory system of the different developmental stages.
2. Materials and methods
2.1. Animals and habitat conditions
Cancer magister megalopas, juveniles and adults were caught and maintained as
previously described (Terwilliger and Brown, 1993). Mudflat and SW salinity and temperature were measured using a refractometer (American Optical) and a thermometer at various tide stages in the Coos River estuary.
2.2. Oxygen uptake
uptake by immersing the respirometers in a thermostated recirculating water bath. All oxygen uptake measurements were made during natural daylight hours. Respirometers were shielded in styrofoam coolers so crabs were not exposed to visual stimuli during the measurement period and the illumination was dim natural daylight.
The rate of change of oxygen concentration in the sealed respirometer was measured with either a YSI Model 5739 oxygen probe and a YSI Model 57 dissolved oxygen meter or a YSI Model 5420A oxygen probe (stirring boot removed) and a YSI Model 54 dissolved oxygen meter. Each chamber was stirred to mix the water and avoid depletion of oxygen adjacent to the electrode. The crabs were shielded from the magnetic stirbars by a mesh frame over the stirbars. Control respirometers, without crabs, were also measured to account for any change in oxygen concentration due to microorganisms or other potential chamber effects. There were no significant changes in oxygen con-centration in the controls.
Food was withheld from the animals for 24 h prior to measurement of oxygen uptake rates to ensure that the animals were in a post-absorptive state and to reduce fouling of the respirometers. Animals were transferred from the holding aquaria (30–33 ppt at 9–158C, with a natural light:dark cycle) into the respirometers immediately prior to the experiments. Animals remained in the respirometers for the entire 8-h measurement period. The crabs were able to move freely around the respirometer chambers. The megalopas swam nearly continuously, while there were brief periods of locomotor activity in the other stages. During this time the respirometers were reoxygenated at regular intervals by bubbling air through the chambers. This was done to ensure that the oxygen levels in respirometers would not become limiting. The oxygen uptake was measured during the first, third, fifth and eighth hour (Fig. 1a). For the fifth instar juvenile and adult crabs, the 1-h measurement periods were interspersed with aeration times (Fig. 1b and c). Within these shorter periods the rates measured for each interval were pooled to give an average rate of oxygen uptake for the hour. For each life stage examined there was a small, but statistically insignificant decline in oxygen uptake over the 8-h acute exposure to the various salinity and temperature combinations. Therefore, the rate of oxygen uptake during the final hour of exposure was used for further consideration.
A wet weight for each individual was determined at the end of the 8-h experiment, after the animal was blotted on paper towels to drain the branchial chambers. Megalopas ranged from 0.033 to 0.055 g (3–4 mm carapace width), first instar juveniles were 0.065 to 0.125 g (6–8 mm carapace width), fifth instar juveniles were 2.53 to 5.43 g (25–32 mm carapace width) and adults were 278.7 to 495.4 g (120–144 mm carapace width).
2.3. Calculation of cardiac output
Cardiac output for each developmental stage in the different salinity and temperature treatments was calculated using the Fick principle:
VO2
]]]]
Vb5(C 2C ) (1)
aO2 vO2
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Fig. 1. Schematic diagram of the timing of measurement of oxygen uptake and aeration intervals. (a) Measurement and aeration periods from 0 to 8 h during acute exposure to salinity and temperature treatments. (b) Measurement periods within each hour measurement interval for 5th juveniles. (c) Measurement periods within each hour for adults.
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oxygen uptake in ml O g2 h ; CaO2 and CvO2 are the oxygen content of the post and 21
prebranchial hemolymph in ml O2 dl hemolymph. Values for CaO2 and CvO2 were derived from the following: (1) oxygen carrying capacity of the hemolymph of the different life stages of C. magister (Brown and Terwilliger, 1998), (2) averaged in vitro hemocyanin oxygen dissociation curves determined at ion concentrations equivalent to those in megalopas and crabs in 50 and 100% SW at 10 and 208C (Terwilliger and Brown, 1993) and (3) values for PaO2 (91 mmHg) and PvO2 (21 mmHg) from Johansen et al. (1970). It should be noted that these PO2values are an extrapolation to the internal conditions of the crabs and megalopas in this study. These values could change with developmental stage, and in response to changes in environmental salinity and temperature. The results of the calculations are nonetheless informative in terms of identifying potential limitations or capacities of the respiratory and circulatory systems.
2.4. Data analysis
of covariance (ANCOVA). Multiple comparison of means were made using the Tukey– Kramer method to determine the minimum significant difference (MSD). Statistical significance was accepted at P,0.05. Statistical analyses were done using SYSTAT version 4.1 (Systat).
3. Results
3.1. Habitat conditions
The mudflat environment frequently utilized by the juveniles in the summer was exposed to changes in temperature from 108C when the tide was high to 258C when the tide had receded and the mudflats were exposed during the day. At the same time salinity dropped from 32 ppt (100% SW) to 16 ppt (50% SW) as the freshwater lens on the surface passed over the mudflat.
3.2. Oxygen uptake
There is a strong interactive effect of temperature and salinity on the rate of oxygen uptake of the megalopas (Table 1). At 108C there is no significant effect of salinity on the rate of oxygen uptake of the megalopas. At 208C, however, the rate of oxygen uptake rises and is greater in 75 and 50% SW than in 100% SW. The interaction of salinity and temperature is also apparent in the Q10 values at the different salinities; the Q10 values are higher at lower salinity for the megalopas.
The rates of oxygen uptake of the first instar juveniles, fifth instar juveniles and adults are not affected by salinity at either 10 or 208C (Table 1). The first instar juvenile and adult crabs have a pronounced effect of temperature on oxygen uptake (Q10.2). The fifth instar juvenile is less temperature sensitive (Q10,2) in the temperature interval examined.
For all combinations of salinity and temperature the regression of log weight specific oxygen uptake on the log body mass is linear (Fig. 2 and Table 2). The slopes of the regressions are not significantly different among treatments. The regression constants are significantly different between 10 and 208C treatments.
3.3. Cardiac output
Weight specific cardiac output is affected by both salinity and temperature (Table 3).The effects, especially of temperature, on cardiac output are greater on the megalopa and juvenile stages than on the adult. The regression of log cardiac output on the log average body mass for each life stage examined yields a linear relationship (Table 4).
4. Discussion
Table 1
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Weight specific rates of oxygen uptake (VO26S.D.; ml O g2 h ) and temperature coefficients (Q ) for four10
life stages of C. magister
Stage Seawater 108C 208C Q10
(%)
VO2 n VO2 n
Megalopa 100 0.990 10 1.676 9 1.69
60.106 60.171
75 1.060 10 2.380 10 2.25
60.051 60.076
50 1.057 10 2.156 9 2.04
60.060 60.222
1st juvenile 100 0.386 12 1.582 10 4.10
60.067 60.079
75 0.497 10 1.483 10 2.98
60.025 60.078
50 0.538 10 1.442 10 2.68
60.038 60.113
5th juvenile 100 0.102 8 0.157 6 1.54
60.026 60.010
75 0.082 8 0.146 8 1.78
60.013 60.010
50 0.093 6 0.152 8 1.63
60.015 60.013
Adult 100 0.028 4 0.060 4 2.14
60.004 60.010
75 0.023 4 0.065 4 2.83
60.005 60.007
50 0.026 3 0.057 4 2.19
60.003 60.006
variety of changes in oxygen uptake are possible in organisms in response to declining partial pressure of oxygen (Mangum and Van Winkle, 1973). They can be classified as either oxyconformers, where the rate of oxygen uptake decreases with declining oxygen tension; or as oxyregulators, where the rate of oxygen uptake is independent of declining oxygen tension down to some critical level at which point the rate of oxygen uptake decreases. Using a mask set-up, Johansen et al. (1970) showed that adult C. magister is an oxyregulator over a very broad range of oxygen tension. In a closed respirometer the difference between an oxyconformer and an oxyregulator is evidenced by either a curvilinear change in oxygen content of the respirometer (an oxyconformer) or a straight line decrease in oxygen content (an oxyregulator). At no time in this study did the rate of decrease in oxygen content in the respirometers for any stages approach a curvilinear pattern.
The rates of oxygen uptake reported here should be regarded as a measure of routine metabolism (McMahon and Wilkens, 1983; Booth and McMahon, 1992). The rates of oxygen uptake reported for unrestrained adult C. magister at 8 and 108C range from
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Fig. 2. Relationship between log weight specific rate of oxygen uptake and log wet weight in C. magister from megalopa (0.033 g) to adult (495.4 g) at; (a) 100% SW, 108C; (b) 75% SW, 108C; (c) 50% SW, 108C; (d) 100% SW, 208C; (e) 70% SW, 208C and (f) 50% SW, 208C.
correspond very closely to the values reported in the present study (Table 1). Comparison between adults of different species of the same magnitude in size reveal similar rates of oxygen uptake. Aldrich (1975) and Aldrich and McMullan (1979) report
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oxygen uptake rates of 0.007 to 0.018 ml O g2 h for Cancer pagurus in the weight range of 336 to 640 g at 108C.
Regression coefficients of the log weight specific oxygen rate versus log body mass for crustaceans reported in the literature span a fairly broad range of values. Dehnel (1960) stated that the regression coefficient depends on a number of factors including the thermal and salinity history of the animals used. He gave regression coefficients
Table 2
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Regression equations for log of weight specific oxygen uptake (V ; ml O gO2 2 h ) vs. log of wet weight (W; g) for C. magister (0.033 g megalopa to 495.4 g adult) at various combinations of salinity and temperatures
Regression equations Salinity Temperature
(% SW) (8C)
2
log VO 25 20.383 (log W )20.741 (R 50.767) 100 10
2
log VO 25 20.440 (log W )20.691 (R 50.921) 75 10
2
log VO 25 20.433 (log W )20.670 (R 50.937) 50 10
2
log VO 25 20.416 (log W )20.326 (R 50.935) 100 20
2
log VO 25 20.435 (log W )20.317 (R 50.921) 75 20
2
Table 3
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Estimated cardiac output (V : ml hemolymph gb h ) based on Fick equation for four life stages of C.
magister
ranging from 20.685 to 20.333 for Hemigrapsus nudus and H. oregonensis under a variety of salinity and temperature conditions. Weymouth et al. (1944) reported a coefficient of 20.2 for Pugettia producta; Roberts (1957) reported a coefficient of
20.336 for Pachygrapsus crassipes. In the current study the regression coefficients (Table 2) are well within the range of values reported for other crabs. The weight range of crabs used in the present study spans a much broader range than any of the other reports cited here. Despite morphological and developmental changes over this broad size range, the underlying relationship between size and metabolic rate is consistent.
Kinne (1964) outlined four different metabolic responses to salinity: type 1, metabolic rate increases in salinity less than the normal range and / or decreases in salinity higher than normal; type 2, metabolic rate increases in salinities below or above the normal salinity range; type 3, the rate decreases in salinities below or above normal salinity range; and type 4, metabolic rate is not affected by changes in salinity. Carcinus maenas exhibits a type 1 or 2 response, oxygen uptake increased at lower than normal salinities (Taylor, 1977). Callinectes sapidus at 208C has an oxygen uptake rate of 0.034 ml O2
21 21
g h in SW at 30 ppt while oxygen uptake is significantly higher at lower salinity, 21 21
0.053 and 0.052 ml O g2 h in 20 ppt and 10 ppt SW respectively (Findley et al. 1978). Callinectes sapidus therefore also exhibits a type 1 or 2 response to salinity. In contrast, the rate of oxygen uptake of adult C. magister is independent of salinity at both
Table 4
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10 and 208C (Table 1) and thus can be categorized as exhibiting a type 4 response. The differences between oxygen uptake of Cancer magister and Callinectes sapidus are consistent with the differences in their ionic regulatory capacities. Callinectes sapidus maintains a more hyperionic hemolymph at reduced salinity (Mangum and Amende, 1972; Colvocoresses et al. 1974) than Cancer magister. The first and fifth instar juveniles of C. magister also fit the type 4 response to salinity at both 10 and 208C (Table 1). Megalopa oxygen uptake, however, is affected by salinity at 208C in a type 1 or 2 fashion, an increase in metabolic rate at subnormal salinities.
Generally, oxygen consumption increases with increasing temperature in ectotherms. A Q10 of 1.0 indicates thermal insensitivity, whereas a Q10 of 2.0 means that the rate function doubles for every 108C increase in temperature. Q10 values may also vary with acclimation temperature (Cossins and Bowler, 1987). The Q10 values for all of the life stages of C. magister studied here (Table 1) are well within the usual range of values for ectotherms.
The remarkable changes in response to salinity and temperature at metamorphosis from megalopa to juvenile C. magister coincide with the transition from oceanic residence to estuarine and coastal areas. Megalopas are only moderately sensitive to temperature but they are quite sensitive to salinity at higher temperature. Upon entering the bay, from the relatively constant oceanic waters, the megalopas rapidly metamorph-ose into first juvenile crabs. The metabolism of the first juvenile at high temperature is less sensitive to decreases in salinity and they may therefore be better suited to the more changeable estuarine waters than the megalopas. In the bay an increase in temperature on the mudflats is likely to be correlated with a decline in salinity as the tide recedes, and so it is unlikely that the juveniles would commonly experience the combination of high temperature and 100% SW that results in a Q10 value of 4.1. A Q10 value this high is far higher than the usual range of 2–3. Extreme sensitivity to temperature means that exposure to high environmental temperatures is metabolically very costly. It may be that temperature sensitivity among first instar juveniles is not selected against since it seems very unlikely that they would encounter high temperature in high salinity. On the other hand, the fifth instar juvenile, the stage many of the Coos estuary crabs have reached by mid-summer, July and August, has a consistently low Q . The fifth instar juvenile10 would actually be exposed to the extremes of high temperature and salinity fluctuations. A reduced sensitivity to temperature over the seasonal extremes may be important in the ability of these young crabs to spend a portion of their time hidden on the mudflats at high temperatures, during daylight low tides; and foraging on the flooded mudflats at high tide, under conditions of low temperature. The ability to utilize the exposed mudflat habitat with a minimal increase in metabolic expense may allow the fifth instar juvenile crabs to exploit a refuge from the aquatic predators, including older crabs, that are concentrated in the channels at low tide.
and estuarine waters in the summer months. The 01 juveniles were more sensitive to temperature in the low part of the temperature range (6–108C) studied than the 11
juveniles. Over the range from 10 to 188C the 01 crabs showed less temperature sensitivity than the 11 crabs. In our study, we have examined two instars within the 01
year class in the Coos estuary, the first instar (6–8 mm carapace width) and fifth instar (25–32 mm carapace width) juveniles, and measured their responses over the 10 to 208C range for the duration of an 8-h tidal cycle. The first instar juvenile showed a greater sensitivity to temperature than the fifth instar juvenile, indicating that between settlement and the end of the first summer, the young crabs undergo a decrease in temperature sensitivity.
As noted by Wheatly (1988), an increase in the rate of oxygen uptake due to salinity stress may not be due solely to an increase in energy expended in ionic and osmotic regulation, but may be due partly to alterations in ventilation, perfusion and changes in other processes related to gas exchange and oxygen transport in the hemolymph. In C.
magister, however, we see no increase in metabolic rate in the first and fifth instar
juveniles and the adults. Only the megalopas show ‘salinity stress’: an increased rate of oxygen uptake as salinity is decreased at 208C.
One parameter that can be used to examine circulatory responses to environmental changes is cardiac output. In this study, the cardiac output calculated for adult C.
21 21
magister in 100% SW at 108C, 4 ml hemolymph g h , is comparable to those 21 21
previously reported for C. magister, 4.3 ml hemolymph g h (McMahon et al., 1979) 21 21 and a congener of similar size, Cancer productus, 3.6 ml hemolymph g h (deFur and McMahon, 1984). Although these earlier studies used other techniques to measure oxygen consumption, these values for cardiac output were all based on calculations using the Fick principle.
In reduced salinity the adult C. magister are regulating hemolymph osmotic and ionic levels (Brown and Terwilliger, 1992). Ion regulation is a metabolically costly process, yet we see no effect of reduced salinity on oxygen uptake of adults. Likewise, we see no effect of salinity on the calculated cardiac output because of (1) no change in oxygen uptake, and (2) no change in hemolymph ion concentrations, especially magnesium and calcium, and therefore maintenance of the hemocyanin functional properties. Conse-quently, we see no apparent change in the cost of perfusion as a result of decreased salinity. It is possible that the apparent lack of metabolic cost for adult crabs exposed to reduced salinity is the result of a shift in allocation of metabolic resources not evident in 1 1 whole animal oxygen consumption measurements. There are costs in terms of Na –K ATPase activity and other ion regulatory mechanisms, therefore there must be a concomitant decrease in energy devoted to some other physiological process. Study of this level of physiological integration was not within the scope of this investigation, but represents a necessary next step in understanding the response of organisms to environmental changes.
Recently McGaw and McMahon (1996) reported cardiac output for adult C. magister (500–800 g), after acute exposure to reduced salinity at 128C, based on pulsed Doppler flow measurements in the five arterial systems leaving the heart. Based on these measurements the cardiac output of an adult crab in 100% SW at 128C was 1.2–2.2 ml
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cardiac output to 0.9–1.4 ml hemolymph g h in crabs acutely exposed to 50% SW for 6 h. McGaw and McMahon (1996) suggest that perfusion of the tissues is declining as the crabs are exposed to reduced salinity. A lower perfusion rate would mean the hemolymph has a greater residence time in the tissues and the gills, allowing a greater level of extraction of oxygen from the water at the gills, assuming an increase in ventilation rates. Greater residence time in the tissues would increase delivery of oxygen from the hemolymph to the tissues. Thus oxygen delivery could be maintained with a reduction in the metabolic costs of pumping hemolymph.
DeWachter and Wilkens (1996) reported an increase in cardiac output from¯1.0–1.6
21 21 21 21
ml hemolymph g h at 128C to¯1.6–2.4 ml hemolymph g h at 208C, and a Q10 value of between 1.66 and 1.8. We show a similar result, with slightly smaller effect of temperature on cardiac output of adult crabs (Table 3).
For the megalopas and juveniles there are increases in calculated cardiac output at low salinity and high temperature, but no consistent trend at 108C. Based on the reduction in oxygen affinity of the hemocyanin due to decreased hemolymph ion concentrations (Terwilliger and Brown, 1993; Brown and Terwilliger, 1992) and the large increases in oxygen uptake at high temperature and / or low salinity, cardiac output is higher under these extreme conditions of high temperature and low salinity. The megalopas and juveniles, especially the first juvenile, would be expected to be very near their limit of respiratory and circulatory capacities as a result of the tidal changes in salinity and temperature in the intertidal estuarine habitat.
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