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Effects of pressure and temperature on the respiration of euphausiids
Deep-SeaResearch,1967,Vol. 14, pp. 725 to 733. PergamonPressLtd. Printedin GreatBritain.
Effects of pressure and temperature on the respiration of euphausiids ~ JOHN M. TEAL'~ and FRANCIS G. CAREYt (Received 27 June 1967) Abstract--The respiration of Euphausia americana, E. hemigibba, E. recurva, Thysanopoda monacantha, T. obtusifrons, T. tricuspidata, and Meganyctiphanes norvegica was measured at temperatures between 5° and 25°C and at pressures between 0 and 100 arm. In most cases the pressure significantlyincreased respiration only at the higher temperatures, a combination of factors not found in the ocean. In T. monacantha, the only mesopelagic species used, pressure increased respiration at the lower temperatures more than at the higher temperatures. We conclude that the respiration of epipelagic forms is determined by temperature alone and decreases as the animals descend into colder waters, while the respiration of the mesopelagic form remains constant throughout its depth range. INTRODUCTION EUPHAUSIIDSare one of the important groups of animals in the oceans which migrate over extensive vertical distances every day. These migrations take them through temperature changes of 10 ° to 15°C and pressure changes of up to 100 atmospheres. These changes are experienced in the course of a few hours in the evening when the animals are swimming up into higher temperatures and lower pressures and the reverse changes are experienced in the early morning (BRINTON, 1962). The effects of changing temperatures on the metabolism of animals is well documented but the effects of changing pressure have been little studied. The only study of the combination of the effects of changing pressure and temperature is that of NAPORA (1964) who worked on the pelagic decapod, Systellaspis debilis. He showed that the effects of increasing pressure increased metabolism by just enough to offset the effects of decreasing temperature so that as the animals varied their depth in the ocean their metabolism remained constant. It has been suggested by MCLAREN (1963) that migrating Crustacea make use of the lower temperatures at depths to slow their metabolism and conserve energy during the day. We have made shipboard measurements on freshly collected euphausiids in the tropical Atlantic and Indian oceans and on one species f r o m the North Atlantic. We found that for forms that migrate into the upper 200 meters the effects of pressure are slight in nature and that the respiratory rate is determined mostly by temperature. METHODS Collections were made with a 2-meter net having mesh openings of 2 × 5 m m using a 4-gallon plastic bucket to close the cod end. Once the animals reached the *Contribution No. 1832 of the Woods Hole Oceanographic Institution, This work was supported by National Science Foundation Grant GB-539 and was part of the U.S. Program in Biology, IIOE, NSF, Grant G-20952. tWoods Hole Oceanographic Institution, Woods Hole, Massachusetts 725
726
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I r
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TO RECORDER
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---, ,M~- ELECTRODEI/, %
STIRRING MAGNET
¢ S >///VA V / / / / , ,
Fig. 1. Diagram of the pressure apparatus showing a euphausiid in position for respiration measurements. bucket, they were protected from damage and were in excellent condition upon reaching the surface. Tows were made either at midnight or 4 a.m. for about 30 rain between 200 m and the surface. The adults and near adults were separated into plastic dishes and stored in a refrigerator. Small larval stages were rejected. Animals were used no later than 1 day after collection. Individual animals were placed in glass vials containing from 15 to 30 ml fresh sea water filtered through 0-45 tz Millipore ® filters and re-aerated (Fig. 1). A piece of plastic screen was held above the animal in the vial by nibs on the glass and a stirring bar rested on the screen., The vial was closed with an oxygen electrode in a rubber stopper. A hypodermic needle through the stopper provided pressure relief during the stoppering procedure. We made the electrodes according to the design of KANWlSlqrR (1959). The vials with their animals were placed in a pressure vessel made of high strength aluminum (7075-T6) with electrical connections to the outside (Connectors No. 2214, Mecca Cable Co.). The pressure vessel was surrounded by six electromagnets connected to a rotating switch which provided a 300 rev/min rotating field for stirring. The whole apparatus was immersed in a temperature controlled water bath. Pressure was applied with a hand operated Blackhawk hydraulic pump through
Effectson pressure and temperatureon the respiration of euphausiids
727
an oil-water separator which prevented oil from entering the vessel containing the animal vials. The voltage drop across a ten-turn, 5000 £2 potentiometer in series with each electrode was fed into a multipoint recorder. This arrangement enabled us to adjust the electrodes individually to indicate full scale on the recorder for air saturated water at the experimental temperature. This was done at the beginning of each experiment. Increases in pressure decrease the electrode output (by 10-15 %/100 arm) and shift the position of the curve which was then returned to its original position by adjusting the potentiometer. Respiration was taken from the slope of the pOz--time curve. The oxygen pressure in the vials was not allowed to fall below 50 ~o air saturation which was not low enough to affect the euphausiids' respiratory rates. Experiments in which the animals respiration slowed markedly during the experiment were rejected. To observe the effects of changing the pressure on the behavior of the euphausiids, we replaced the metal cap with one of lucite through which we could observe the animals. For reasons of safety, there were no electrical leads through the plastic so that we could not observe animals and record their respiration simultaneously. We put the animals in the pressure vessel and watched the record until a steady respiratory rate was achieved, then alternated the pressure between two values at 10-30 rain intervals, leaving it at one level long enough to get an accurate reading of the respiratory rate before and after each pressure change. This was repeated at a series of constant temperatures at 5°C intervals from 5°-25°C. The respiration of more than one animal was measured at each temperature. In some cases the animals were preserved in neutral formalin and later weighed ashore allowing us to calculate respiratory rates. In others only the relative changes in respiratory rate were determined. Rates and relative changes were measured with an accuracy of better than 10 Yo. Since size and respiration are linearly related in the euphausiids where this has been investigated (SMALLet al., 1966) and since our specimens within any one species varied in size by no more than a factor of two, we made no size correction when calculating weight specific rates. The rotating magnetic field and the rotating stirring bar did not affect the measured rates as was shown by doing four experiments with the magnets turned off. The pressure was not changed because the electrode response was slow without stirring. The respiratory rates were not significantly different from those in regular stirred runs. Measurements were also made in an open, plastic water bath where the animals could be observed during experiments with temperature changes only. When the animals were weighed, respiratory rates were calculated on a weight basis along with their standard deviations and errors. Since weights were not available in all cases, we used relative changes in respiratory rate to calculate the probability that a change in pressure was followed by a change in respiratory rate. If there were no significant effect of pressure, then the rates would as likely increase as decrease. The number of experiments in which the rate increased was compared with the number in which the rate decreased and the binomial distribution used to test the significance of the difference between the two groups. The number of experiments in which the change was not measurable, which was always less than the difference between the number of increases and of decreases, was combined with the smaller of these groups which minimized the probability of a significant difference between them. This calculation assigns a probability to the statement that pressure causes a change in rate but
728
J o h n M. TEAL and FRArqcls G. CAp.~Y
says nothing about the amount of change. The significance of the amount of change must be inferred from the statistics on the rate per unit weight calculations. RESULTS
Visual observations showed that the euphausiids were apparently unharmed by pumping the pressure to 350 atm as fast as possible, about 30 see, or by sudden decompression from 400 atm in 1 sec. After a sudden, largepressure change the euphausiids swam in the vial for up to 5 min and then remained quiet, lying on the bottom of the vial fanning their pleopods. After smaller changes as used in the respiratory mea-
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Fig. 2. Respiration of Euphausia species at various pressures and temperatures. The vertical lines through the points indicate the standard error of the mean. The number in parenthesis beside the vertical line is the number of weight-specific respiration determinations. The number over the line is the probability that change in pressure consistantly produced an increase or decrease in respiration. The number in parenthesis beside the probability is the number of deteiminations. In cases where weight specific rates were not determined, dotted lines indicate the range between the greatest increase and greatest decrease in respiration produced by that pressure change. The positions of the zero pressure points were determined from measurements made in a water bath at room pressure from which the Q 10's were calculated.
Effects of pressure and temperature on the respiration of euphausiids
729
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Fig. 3. Respiration of species of Thysanopoda. Explanation as in Fig. 2. surements, the initial period of swimming was usually shorter than 30 sec and was easily distinguished from the rest of the record and not used in calculating rates. Respiratory rates were similar to those reported by other investigators using various methods (SMALL et al., 1966; LAsrdzR, 1966). Respiratory data were obtained for Euphausia americana, E. brevis, Thysanopoda monacantha, and T. tricuspidata in the tropical Atlantic; for Meganyctiphanes norvegica in the North Atlantic; and for E. hemigibba, E. recurva, T. obtusifrons, T. monacantha, and T. tricuspidata in the Mozambique Channel. Unfortunately, since we worked from a ship at sea, it was not always possible to catch the same species day after day. The data have gaps therefore and for no species do we have a complete set of records at all the experimental temperatures and pressures.
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730
Jon~ M. TEAL and FRANCISG. CAREY
In four species there was some increase in respiratory rate as pressure was increased (Figs. 2-4). E. recurva, for which we have data only at 15°C, had a respiration that increased 1.9/100 arm. E. hemigibba's respiration increased 1.5/100 atm. at 25 ° and 1,2/100 atm at 20 ° and the respiration of T. tricuspidata increased 1"2/100 arm at 20 °. At lower temperatures the latter two species showed no increase in respiration when pressure increased. T. monacantha showed an increase of 2.3/100 atm at 10° but no significant change at 20 ° where the scatter in points was rather large. Only in the case of Meganyctiphanes was there a significant decrease in respiration with increasing pressure, respiration at 100 atm was 0"76 of that at 1 atm. In all other cases, Meganyctiphanes at 10°, T. monacantha at 20 °, T. obtusifrons from 10° to 20°C, T. tricuspidata at 10° and 15°C, E. hemigibba at 10°, and E. americana at 15° and 25 ° there was no significant change in respiratory rate with changing pressure. All of the species exhibited a relationship between respiratory rate and temperature that gave a straight line on a semi-log plot and yielded Q 10's that varied from 2.0 to 3.5. The animals often spent short periods swimming, especially at the beginning of an experiment. This could be seen in the measurements done in the water bath and was inferred from the records of experiments in the pressure vessel. From ten such observations taken during two successive days, we found the respiration during swimming was about 3 × (range 2-4) the resting rate, when the euphausiids lay at the bottom of the vial fanning their pleopods. DISCUSSION
In slightly less than half of the curves presented here, there is a relationship between M M JO2 / G M HR. 0
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Fig. 5. Respiration of euphausiids plotted against depth using the indicated depth-temperature distribution which is typical of summer, open ocean conditions. The solid symbols indicate respiration determined solely by temperature. Where pressure has a significant effect, an open symbol
includes the effect of both factors.
Effects of pressure and temperature on the respiration of euphausiids
731
respiration of the euphausiids and pressure within the range which the animals might experience in the sea; i.e., 1-100 arm. However, most of these pressure effects are significant only at temperatures that are encountered at the surface of the oceans. At the lower temperatures that occur wherever high pressures are found, most of the pressure effects that were discovered were insignificant. By plotting the respiration of these euphausiids against depth and assuming a temperature distribution typical of a tropical ocean (or a temperate ocean in summer), we can demonstrate the relative effects of temperature and pressure (Fig. 5). The solid lines indicate the respiratory rates of the euphausiids as they would be if pressure had no effect and the respiratory rates were determined only by temperature. The dotted lines include the effect of pressure on the rates. In only two cases does the respiratory rate change significantly under the influence of pressure. The respiration of 7". monacantha is increased by pressure so that below 100 m the respiration is approximately constant regardless ofthe depth. On the other hand, the respiration of Meganyctiphanes is slightly decreased by pressure so that at 1000 m it is slightly lower than it would be if there were no pressure effect. In all other combinations of animals reported on here and temperature and pressure as found in the oceans, the respiration is determined by temperature alone. MCLAR~N (1963) has suggested that scattering layer organisms which can obtain enough food for 24 hr by feeding only at the surface at night, can save energy which might otherwise be expended by descending and spending the day at the lower temperatures found below the surface. The savings are diverted to growth and reproduction. Although development will be slower because half of the animals life is spent in colder waters, a seasonal breeder could advantageously trade slower development for greater ultimate fecundity. For the savings to be significant, however, the temperature difference between the night and day levels must be large enough so that the metabolism during the day is reduced by more than enough to offset the effort of the twice daily migration. If we take the data for E. hemigibba to represent a typical case we can calculate what a euphausiid might save by migrating. In this we ignore any possible effects of changes in metabolic substrate. If E. hemigibba stayed at the surface all day it would consume 22.8 ml O~/g/day at a surface temperature of 25°C. We shall assume a temperature distribution like that indicated in Fig. 2, and that it takes the animals about 2 hr to migrate from the surface to 500 m where they spend the day. This is consistent with observed rates of movement of the scattering layer and with measured swimming speeds ofeuphausiids (HARDYand BAINBRIDCE,1954). We shall also assume that during the migration period the euphasiids respire at three times the rates which we measured for animals resting in the vials. (Active animals respired at about 3 × the rate of resting animals). With these assumptions, if the animals spend 12 hr at 500 m and the other 12 hr migrating and feeding at the surface, they would consume 15.1 ml O2/g/day or save an amount equivalent to the consumption of 7.7 ml Oz/g/day. Since the animals weigh about 50 mg this is a saving of 0.35 ml per individual which is equivalent to the oxidation of the amount of food contained in one copepod weighing about 2 mg. A similar calculation for Meganyctiphanes norvegica migrating from 100 to 500 m indicates a saving of 0.24 ml O~/day for an individual of 200 mg fresh weight. However, in this species the saving due to the lower temperature at depth is enhanced by a
732
JOHNM. TEALand FRANCtSG. CAREV
reduction in metabolism due to pressure and results in a total saving of 0.38 ml O2/day or about the same as we calculated for the tropical species. The average temperature difference through which M. norvegica migrates is less than the average experienced by the more tropical species since the surface waters in the north reach the high temperatures used in these calculations only in late summer. Our data are insufficient to serve as the basis for a more exact calculation of actual respiratory savings, but they suggest that the pressure effect is about enough to give the northern form the same changes in respiration experienced by the tropical forms. All of the euphausiids used in this study are classed as epipelagic by BRINTON (1962) and migrate to the surface at night, with the exception of T. monacantha which is considered to be mesopelagic and does not come to within 150 m of the surface at night. Our data indicate that in their normal range, T. monacantha have constant metabolism and do not make any saving by migrating. In fact they will spend 15-20 ~ more energy by migrating than they would by staying at one depth for the full 24 hr. T. monacantha was the only mesopelagic species that we caught in sufficient numbers for determinations, but the data of NAI'ORA(1964) for a mesopelagic decapod Systellaspis debilis suggest that a constant metabolism throughout normal depth range might be a general feature of mesopelagic Crustacea. McLaren's hypothesis will not fit these animals and there must be some other reason for their migration which is consistent with their constant metabolic rate. The mesopelagic Crustacea do not come into the surface layers where the phytoplankton is most abundant and are not likely to be herbiverous. Their mandibles have well developed incisor portions as well as the grinding molar parts (as have many of the epipelagic forms). The area between the bases of the limbs where collected food is held before being passed to the mandibles as well as the stomachs of the dozen specimens we have looked at, contained a mass of unidentifiable material as did the euphausiids examined by EINARSSON(1945). Animals confined in dishes have been observed to catch and eat smaller euphausiids occasionally. MAUCHLINn(1960, 1966) reported that Meganyctiphanes and Thysanoessa species eat animals although in the shallow water of the Clyde Sea where he collected, these animals were on the average more than half full of detritus. CHACE(1940) reported that the mesopelagic decapods common off Bermuda had recognizable portions of fish and Crustacea as well as amorphous material in their stomachs. All this suggests that these animals feed on anything that comes their way from live prey to detritus and perhaps fecal pellets. In any case, since the mesopelagic forms do not come into the euphoric layer, their food is less concentrated than that fed on by the epipelagic forms and perhaps the deeper living kinds cannot depend on getting enough food during the night to last through the 24 hr. If we suggest that the mesopelagic forms keep their metabolism constant because they must feed throughout the day, the question immediately arises as to why they migrate at all. Since migration uses extra energy, we may suppose that it has been retained because it has some positive value for the animals' survival. Perhaps the mesopelagic forms get most food when remaining just below their food source, in a suitable position to intercept sluggish and dead individuals and detritus and feces resulting from feeding activities above them. There is no indication from our results that the higher temperature at the surface is harmful to them. We can say nothing further as so little is known of the habits, ecology, and
Effects of pressure and temperature on the respiration of euphausiids
733
physiology of these animals. We guess that the maintenance of a constant metabolism regardless of depth has something to do with food and feeding habits. Our data for epipelagic euphausiids are consistent with McLaren's hypothesis that scattering layer organisms migrate to conserve energy. Their metabolism is determined almost exclusively by temperature and pressure either has little effect or emphasizes the effect of the temperature distribution. Mesopelagic forms probably constitute a physiologically distinct group and maintain constant metabolism regardless of depth. REFERENCES
BRINTON E. (1962) The distribution of Pacific euphausiids. Bull. Scripps Inst. Oceanogr., 8, 51-269. CHACE F. A., Jr. (1940) Plankton of the Bermuda Oceanographic Expeditions. IX. Bathypelagic caridean Crustacea. Zoologica, 25, 117-209. EINARSSONH. (1945) Euphausiacea I. North Atlantic species. Dana Rept., N27, 1-185. HARDYA. C. and R. BAINBRID~E(1954) Experimental observations on the vertical migrations of planktonic animals. J. mar. Biol. Ass. U.K., 33, 409--448. KhNWnSrIERJ. W. (1959) Polarographic oxygen electrode. Limnol. Oceanogr., 4, 210-217. LASKER R. (1966) Feeding, growth, respiration, and carbon utilization of a euphausiid crustacean. J. fish. Res. Bd. Canada, 23, 1291-1317. MAtrCHLrNE J. (1960) The biology of the euphausid crustacean, Meganyctiphanes norvegica (M. Sars). Proc. R. Soc. Edinb., Ser. B. 67, 141-179. MAOCHLr~,r~J. (1966) The biology of Thysanoessa raschii (M. Sars), with a comparison of its diet with that of Meganyctiphanes norvegica (M. Sars). In : Some studies in contemporary marine science, H. BARN~S,editor, pp. 509-528. Allen & Unwin, London. McLAR~N I. A. (1963) Effects of temperature on growth of zooplankton, and the adaptive value of vertical migration, d. fish Res. Bd. Canada, 20, 685-727. NAPORh T. A. (1964) The effect of hydrostatic pressure on the prawn, Systellapsis debilis. Narragansett Mar. Lab. Occ. Publ., 2, 92-94. SMALLL. F., J. F. HEBARDand C. D. MClNTIRE(1966) Respiration in euphausids. Nature, Lond., 211, 1210-1211.
Effects of pressure and temperature on the respiration of euphausiids ~ JOHN M. TEAL'~ and FRANCIS G. CAREYt (Received 27 June 1967) Abstract--The respiration of Euphausia americana, E. hemigibba, E. recurva, Thysanopoda monacantha, T. obtusifrons, T. tricuspidata, and Meganyctiphanes norvegica was measured at temperatures between 5° and 25°C and at pressures between 0 and 100 arm. In most cases the pressure significantlyincreased respiration only at the higher temperatures, a combination of factors not found in the ocean. In T. monacantha, the only mesopelagic species used, pressure increased respiration at the lower temperatures more than at the higher temperatures. We conclude that the respiration of epipelagic forms is determined by temperature alone and decreases as the animals descend into colder waters, while the respiration of the mesopelagic form remains constant throughout its depth range. INTRODUCTION EUPHAUSIIDSare one of the important groups of animals in the oceans which migrate over extensive vertical distances every day. These migrations take them through temperature changes of 10 ° to 15°C and pressure changes of up to 100 atmospheres. These changes are experienced in the course of a few hours in the evening when the animals are swimming up into higher temperatures and lower pressures and the reverse changes are experienced in the early morning (BRINTON, 1962). The effects of changing temperatures on the metabolism of animals is well documented but the effects of changing pressure have been little studied. The only study of the combination of the effects of changing pressure and temperature is that of NAPORA (1964) who worked on the pelagic decapod, Systellaspis debilis. He showed that the effects of increasing pressure increased metabolism by just enough to offset the effects of decreasing temperature so that as the animals varied their depth in the ocean their metabolism remained constant. It has been suggested by MCLAREN (1963) that migrating Crustacea make use of the lower temperatures at depths to slow their metabolism and conserve energy during the day. We have made shipboard measurements on freshly collected euphausiids in the tropical Atlantic and Indian oceans and on one species f r o m the North Atlantic. We found that for forms that migrate into the upper 200 meters the effects of pressure are slight in nature and that the respiratory rate is determined mostly by temperature. METHODS Collections were made with a 2-meter net having mesh openings of 2 × 5 m m using a 4-gallon plastic bucket to close the cod end. Once the animals reached the *Contribution No. 1832 of the Woods Hole Oceanographic Institution, This work was supported by National Science Foundation Grant GB-539 and was part of the U.S. Program in Biology, IIOE, NSF, Grant G-20952. tWoods Hole Oceanographic Institution, Woods Hole, Massachusetts 725
726
Joi~N M. TEALand FRANCISG. CAREY
I r
!
HYDRAULIC PUMP
/
GAGE
OIL-WATER SEPARATOR
TO RECORDER
¢ ¢ ¢ ¢
_OXYGEN
V I
---, ,M~- ELECTRODEI/, %
STIRRING MAGNET
¢ S >///VA V / / / / , ,
Fig. 1. Diagram of the pressure apparatus showing a euphausiid in position for respiration measurements. bucket, they were protected from damage and were in excellent condition upon reaching the surface. Tows were made either at midnight or 4 a.m. for about 30 rain between 200 m and the surface. The adults and near adults were separated into plastic dishes and stored in a refrigerator. Small larval stages were rejected. Animals were used no later than 1 day after collection. Individual animals were placed in glass vials containing from 15 to 30 ml fresh sea water filtered through 0-45 tz Millipore ® filters and re-aerated (Fig. 1). A piece of plastic screen was held above the animal in the vial by nibs on the glass and a stirring bar rested on the screen., The vial was closed with an oxygen electrode in a rubber stopper. A hypodermic needle through the stopper provided pressure relief during the stoppering procedure. We made the electrodes according to the design of KANWlSlqrR (1959). The vials with their animals were placed in a pressure vessel made of high strength aluminum (7075-T6) with electrical connections to the outside (Connectors No. 2214, Mecca Cable Co.). The pressure vessel was surrounded by six electromagnets connected to a rotating switch which provided a 300 rev/min rotating field for stirring. The whole apparatus was immersed in a temperature controlled water bath. Pressure was applied with a hand operated Blackhawk hydraulic pump through
Effectson pressure and temperatureon the respiration of euphausiids
727
an oil-water separator which prevented oil from entering the vessel containing the animal vials. The voltage drop across a ten-turn, 5000 £2 potentiometer in series with each electrode was fed into a multipoint recorder. This arrangement enabled us to adjust the electrodes individually to indicate full scale on the recorder for air saturated water at the experimental temperature. This was done at the beginning of each experiment. Increases in pressure decrease the electrode output (by 10-15 %/100 arm) and shift the position of the curve which was then returned to its original position by adjusting the potentiometer. Respiration was taken from the slope of the pOz--time curve. The oxygen pressure in the vials was not allowed to fall below 50 ~o air saturation which was not low enough to affect the euphausiids' respiratory rates. Experiments in which the animals respiration slowed markedly during the experiment were rejected. To observe the effects of changing the pressure on the behavior of the euphausiids, we replaced the metal cap with one of lucite through which we could observe the animals. For reasons of safety, there were no electrical leads through the plastic so that we could not observe animals and record their respiration simultaneously. We put the animals in the pressure vessel and watched the record until a steady respiratory rate was achieved, then alternated the pressure between two values at 10-30 rain intervals, leaving it at one level long enough to get an accurate reading of the respiratory rate before and after each pressure change. This was repeated at a series of constant temperatures at 5°C intervals from 5°-25°C. The respiration of more than one animal was measured at each temperature. In some cases the animals were preserved in neutral formalin and later weighed ashore allowing us to calculate respiratory rates. In others only the relative changes in respiratory rate were determined. Rates and relative changes were measured with an accuracy of better than 10 Yo. Since size and respiration are linearly related in the euphausiids where this has been investigated (SMALLet al., 1966) and since our specimens within any one species varied in size by no more than a factor of two, we made no size correction when calculating weight specific rates. The rotating magnetic field and the rotating stirring bar did not affect the measured rates as was shown by doing four experiments with the magnets turned off. The pressure was not changed because the electrode response was slow without stirring. The respiratory rates were not significantly different from those in regular stirred runs. Measurements were also made in an open, plastic water bath where the animals could be observed during experiments with temperature changes only. When the animals were weighed, respiratory rates were calculated on a weight basis along with their standard deviations and errors. Since weights were not available in all cases, we used relative changes in respiratory rate to calculate the probability that a change in pressure was followed by a change in respiratory rate. If there were no significant effect of pressure, then the rates would as likely increase as decrease. The number of experiments in which the rate increased was compared with the number in which the rate decreased and the binomial distribution used to test the significance of the difference between the two groups. The number of experiments in which the change was not measurable, which was always less than the difference between the number of increases and of decreases, was combined with the smaller of these groups which minimized the probability of a significant difference between them. This calculation assigns a probability to the statement that pressure causes a change in rate but
728
J o h n M. TEAL and FRArqcls G. CAp.~Y
says nothing about the amount of change. The significance of the amount of change must be inferred from the statistics on the rate per unit weight calculations. RESULTS
Visual observations showed that the euphausiids were apparently unharmed by pumping the pressure to 350 atm as fast as possible, about 30 see, or by sudden decompression from 400 atm in 1 sec. After a sudden, largepressure change the euphausiids swam in the vial for up to 5 min and then remained quiet, lying on the bottom of the vial fanning their pleopods. After smaller changes as used in the respiratory mea-
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x
mr
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Euphausia
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recurva
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ATMOSPHERES
Fig. 2. Respiration of Euphausia species at various pressures and temperatures. The vertical lines through the points indicate the standard error of the mean. The number in parenthesis beside the vertical line is the number of weight-specific respiration determinations. The number over the line is the probability that change in pressure consistantly produced an increase or decrease in respiration. The number in parenthesis beside the probability is the number of deteiminations. In cases where weight specific rates were not determined, dotted lines indicate the range between the greatest increase and greatest decrease in respiration produced by that pressure change. The positions of the zero pressure points were determined from measurements made in a water bath at room pressure from which the Q 10's were calculated.
Effects of pressure and temperature on the respiration of euphausiids
729
800L Thysanopoda' monacantha olo~z.~ T 6001(6)
.-
~~ ~
4oo1::"" >'' ~,3~ ~ : . . . : ~ tts. ~Z2.-~2q-.(zs) ......... 2 0 0 ~ 0 0 t
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(t7)
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:
I
-Thysenopoda'
I
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obtusifrons
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>'
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~.t(4) . . . .
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, lricusDidata
02(9) 600
200
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Fig. 3. Respiration of species of Thysanopoda. Explanation as in Fig. 2. surements, the initial period of swimming was usually shorter than 30 sec and was easily distinguished from the rest of the record and not used in calculating rates. Respiratory rates were similar to those reported by other investigators using various methods (SMALL et al., 1966; LAsrdzR, 1966). Respiratory data were obtained for Euphausia americana, E. brevis, Thysanopoda monacantha, and T. tricuspidata in the tropical Atlantic; for Meganyctiphanes norvegica in the North Atlantic; and for E. hemigibba, E. recurva, T. obtusifrons, T. monacantha, and T. tricuspidata in the Mozambique Channel. Unfortunately, since we worked from a ship at sea, it was not always possible to catch the same species day after day. The data have gaps therefore and for no species do we have a complete set of records at all the experimental temperatures and pressures.
.~
~(5! ~>~ .I(7)
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Meganyctiphanes norvegica a~o~Z,o
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7;
~8o
TMOSPHERES
Fig. 4. Respiration of Meganyctiphanes. Explanation as in Fig. 2.
730
Jon~ M. TEAL and FRANCISG. CAREY
In four species there was some increase in respiratory rate as pressure was increased (Figs. 2-4). E. recurva, for which we have data only at 15°C, had a respiration that increased 1.9/100 arm. E. hemigibba's respiration increased 1.5/100 atm. at 25 ° and 1,2/100 atm at 20 ° and the respiration of T. tricuspidata increased 1"2/100 arm at 20 °. At lower temperatures the latter two species showed no increase in respiration when pressure increased. T. monacantha showed an increase of 2.3/100 atm at 10° but no significant change at 20 ° where the scatter in points was rather large. Only in the case of Meganyctiphanes was there a significant decrease in respiration with increasing pressure, respiration at 100 atm was 0"76 of that at 1 atm. In all other cases, Meganyctiphanes at 10°, T. monacantha at 20 °, T. obtusifrons from 10° to 20°C, T. tricuspidata at 10° and 15°C, E. hemigibba at 10°, and E. americana at 15° and 25 ° there was no significant change in respiratory rate with changing pressure. All of the species exhibited a relationship between respiratory rate and temperature that gave a straight line on a semi-log plot and yielded Q 10's that varied from 2.0 to 3.5. The animals often spent short periods swimming, especially at the beginning of an experiment. This could be seen in the measurements done in the water bath and was inferred from the records of experiments in the pressure vessel. From ten such observations taken during two successive days, we found the respiration during swimming was about 3 × (range 2-4) the resting rate, when the euphausiids lay at the bottom of the vial fanning their pleopods. DISCUSSION
In slightly less than half of the curves presented here, there is a relationship between M M JO2 / G M HR. 0
200
400
600
800
t000
f 5* 200[
t0"
+
50C
~t.8x
• a Thysanopoda
I
monacanthc
~ T. o b t u s i f r o n s + "E t r i c u s p i d a t a • ~ Meganycfiphanes • Euphausia
~rl 5* t00C - - ~ ' ~
norvegica
americana
• o E. hemigibba 0.8~
I
-L
r
E
Fig. 5. Respiration of euphausiids plotted against depth using the indicated depth-temperature distribution which is typical of summer, open ocean conditions. The solid symbols indicate respiration determined solely by temperature. Where pressure has a significant effect, an open symbol
includes the effect of both factors.
Effects of pressure and temperature on the respiration of euphausiids
731
respiration of the euphausiids and pressure within the range which the animals might experience in the sea; i.e., 1-100 arm. However, most of these pressure effects are significant only at temperatures that are encountered at the surface of the oceans. At the lower temperatures that occur wherever high pressures are found, most of the pressure effects that were discovered were insignificant. By plotting the respiration of these euphausiids against depth and assuming a temperature distribution typical of a tropical ocean (or a temperate ocean in summer), we can demonstrate the relative effects of temperature and pressure (Fig. 5). The solid lines indicate the respiratory rates of the euphausiids as they would be if pressure had no effect and the respiratory rates were determined only by temperature. The dotted lines include the effect of pressure on the rates. In only two cases does the respiratory rate change significantly under the influence of pressure. The respiration of 7". monacantha is increased by pressure so that below 100 m the respiration is approximately constant regardless ofthe depth. On the other hand, the respiration of Meganyctiphanes is slightly decreased by pressure so that at 1000 m it is slightly lower than it would be if there were no pressure effect. In all other combinations of animals reported on here and temperature and pressure as found in the oceans, the respiration is determined by temperature alone. MCLAR~N (1963) has suggested that scattering layer organisms which can obtain enough food for 24 hr by feeding only at the surface at night, can save energy which might otherwise be expended by descending and spending the day at the lower temperatures found below the surface. The savings are diverted to growth and reproduction. Although development will be slower because half of the animals life is spent in colder waters, a seasonal breeder could advantageously trade slower development for greater ultimate fecundity. For the savings to be significant, however, the temperature difference between the night and day levels must be large enough so that the metabolism during the day is reduced by more than enough to offset the effort of the twice daily migration. If we take the data for E. hemigibba to represent a typical case we can calculate what a euphausiid might save by migrating. In this we ignore any possible effects of changes in metabolic substrate. If E. hemigibba stayed at the surface all day it would consume 22.8 ml O~/g/day at a surface temperature of 25°C. We shall assume a temperature distribution like that indicated in Fig. 2, and that it takes the animals about 2 hr to migrate from the surface to 500 m where they spend the day. This is consistent with observed rates of movement of the scattering layer and with measured swimming speeds ofeuphausiids (HARDYand BAINBRIDCE,1954). We shall also assume that during the migration period the euphasiids respire at three times the rates which we measured for animals resting in the vials. (Active animals respired at about 3 × the rate of resting animals). With these assumptions, if the animals spend 12 hr at 500 m and the other 12 hr migrating and feeding at the surface, they would consume 15.1 ml O2/g/day or save an amount equivalent to the consumption of 7.7 ml Oz/g/day. Since the animals weigh about 50 mg this is a saving of 0.35 ml per individual which is equivalent to the oxidation of the amount of food contained in one copepod weighing about 2 mg. A similar calculation for Meganyctiphanes norvegica migrating from 100 to 500 m indicates a saving of 0.24 ml O~/day for an individual of 200 mg fresh weight. However, in this species the saving due to the lower temperature at depth is enhanced by a
732
JOHNM. TEALand FRANCtSG. CAREV
reduction in metabolism due to pressure and results in a total saving of 0.38 ml O2/day or about the same as we calculated for the tropical species. The average temperature difference through which M. norvegica migrates is less than the average experienced by the more tropical species since the surface waters in the north reach the high temperatures used in these calculations only in late summer. Our data are insufficient to serve as the basis for a more exact calculation of actual respiratory savings, but they suggest that the pressure effect is about enough to give the northern form the same changes in respiration experienced by the tropical forms. All of the euphausiids used in this study are classed as epipelagic by BRINTON (1962) and migrate to the surface at night, with the exception of T. monacantha which is considered to be mesopelagic and does not come to within 150 m of the surface at night. Our data indicate that in their normal range, T. monacantha have constant metabolism and do not make any saving by migrating. In fact they will spend 15-20 ~ more energy by migrating than they would by staying at one depth for the full 24 hr. T. monacantha was the only mesopelagic species that we caught in sufficient numbers for determinations, but the data of NAI'ORA(1964) for a mesopelagic decapod Systellaspis debilis suggest that a constant metabolism throughout normal depth range might be a general feature of mesopelagic Crustacea. McLaren's hypothesis will not fit these animals and there must be some other reason for their migration which is consistent with their constant metabolic rate. The mesopelagic Crustacea do not come into the surface layers where the phytoplankton is most abundant and are not likely to be herbiverous. Their mandibles have well developed incisor portions as well as the grinding molar parts (as have many of the epipelagic forms). The area between the bases of the limbs where collected food is held before being passed to the mandibles as well as the stomachs of the dozen specimens we have looked at, contained a mass of unidentifiable material as did the euphausiids examined by EINARSSON(1945). Animals confined in dishes have been observed to catch and eat smaller euphausiids occasionally. MAUCHLINn(1960, 1966) reported that Meganyctiphanes and Thysanoessa species eat animals although in the shallow water of the Clyde Sea where he collected, these animals were on the average more than half full of detritus. CHACE(1940) reported that the mesopelagic decapods common off Bermuda had recognizable portions of fish and Crustacea as well as amorphous material in their stomachs. All this suggests that these animals feed on anything that comes their way from live prey to detritus and perhaps fecal pellets. In any case, since the mesopelagic forms do not come into the euphoric layer, their food is less concentrated than that fed on by the epipelagic forms and perhaps the deeper living kinds cannot depend on getting enough food during the night to last through the 24 hr. If we suggest that the mesopelagic forms keep their metabolism constant because they must feed throughout the day, the question immediately arises as to why they migrate at all. Since migration uses extra energy, we may suppose that it has been retained because it has some positive value for the animals' survival. Perhaps the mesopelagic forms get most food when remaining just below their food source, in a suitable position to intercept sluggish and dead individuals and detritus and feces resulting from feeding activities above them. There is no indication from our results that the higher temperature at the surface is harmful to them. We can say nothing further as so little is known of the habits, ecology, and
Effects of pressure and temperature on the respiration of euphausiids
733
physiology of these animals. We guess that the maintenance of a constant metabolism regardless of depth has something to do with food and feeding habits. Our data for epipelagic euphausiids are consistent with McLaren's hypothesis that scattering layer organisms migrate to conserve energy. Their metabolism is determined almost exclusively by temperature and pressure either has little effect or emphasizes the effect of the temperature distribution. Mesopelagic forms probably constitute a physiologically distinct group and maintain constant metabolism regardless of depth. REFERENCES
BRINTON E. (1962) The distribution of Pacific euphausiids. Bull. Scripps Inst. Oceanogr., 8, 51-269. CHACE F. A., Jr. (1940) Plankton of the Bermuda Oceanographic Expeditions. IX. Bathypelagic caridean Crustacea. Zoologica, 25, 117-209. EINARSSONH. (1945) Euphausiacea I. North Atlantic species. Dana Rept., N27, 1-185. HARDYA. C. and R. BAINBRID~E(1954) Experimental observations on the vertical migrations of planktonic animals. J. mar. Biol. Ass. U.K., 33, 409--448. KhNWnSrIERJ. W. (1959) Polarographic oxygen electrode. Limnol. Oceanogr., 4, 210-217. LASKER R. (1966) Feeding, growth, respiration, and carbon utilization of a euphausiid crustacean. J. fish. Res. Bd. Canada, 23, 1291-1317. MAtrCHLrNE J. (1960) The biology of the euphausid crustacean, Meganyctiphanes norvegica (M. Sars). Proc. R. Soc. Edinb., Ser. B. 67, 141-179. MAOCHLr~,r~J. (1966) The biology of Thysanoessa raschii (M. Sars), with a comparison of its diet with that of Meganyctiphanes norvegica (M. Sars). In : Some studies in contemporary marine science, H. BARN~S,editor, pp. 509-528. Allen & Unwin, London. McLAR~N I. A. (1963) Effects of temperature on growth of zooplankton, and the adaptive value of vertical migration, d. fish Res. Bd. Canada, 20, 685-727. NAPORh T. A. (1964) The effect of hydrostatic pressure on the prawn, Systellapsis debilis. Narragansett Mar. Lab. Occ. Publ., 2, 92-94. SMALLL. F., J. F. HEBARDand C. D. MClNTIRE(1966) Respiration in euphausids. Nature, Lond., 211, 1210-1211.