Respiration and the effects of pressure on the mesopelagic vertically migrating squid Histioteuthis heteropsis
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1 Limnol. Oceanogr., 23(4), 1978, 1978, by the American Society of Limnology and Oceanography, Inc. Respiration and the effects of pressure on the mesopelagic vertically migrating squid Histioteuthis heteropsis Bruce W. Belman2 Department of Biology, University of California, Los Angeles Abstract The effects of hydrostatic pressure and dissolved oxygen concentration on oxygen consumption rates were examined in the mesopelagic, vertically migrating squid Histioteuthis heteropsis from southern California offshore waters. Elevated hydrostatic pressures (to 136 atm) had no significant effects on oxygen consumption rates at 5 C. Low oxygen concentrations (<0.5 ml Oz*liter- ) depressed rates of oxygen consumption. These findings suggest that metabolism is pressure insensitive during vertical migrations and that at least partial anaerobiosis may be necessary to supply the total energy needs of this species at daytime depths in the oxygen minimum layer off southern California. Recent studies of the effects of temperature and hydrostatic pressure on metabolic rates in open ocean pelagic crustaceans, pteropods, and fishes suggest that patterns of metabolic response to these variables are related both to the distinctive habits of vertical migration or nonmigration of certain groups of species and to the particular hydrographic conditions found within the vertical distributions of these species (Quetin and Childress 1976). In general, epipelagic migrators show different patterns of metabolic response to temperature and pressure than do mesopelagic migrators or mesopelagic nonmigrators. Those species that migrate from oxygen minimum layers into oxygen-rich surface waters also show quite different patterns from organisms that remain in oxygen minimum conditions all of the time (e.g. Meek and Childrcss 1973; Smith and Hessler 1974; Childress 1977). In an effort to provide additional data with which to examine these hypotheses, I report here the effects of hydrostatic pressure and available oxygen concentrations on oxygen consumption rates in the squid Ilistioteuthis heteropsis (Teuthoi- This work was supported by NSF grant PCM to M. S. Gordon (University of California, Los Angeles), GA to J. J. Childress (Univ. California, Santa Barbara), and the Laboratory of Fisheries and Marine Biology (Univ. California, Los Angeles). Present address: th St., Newport Beach, California dea). This squid is a relatively common cold water species with a geographic range from southern California to Mon- terey Bay (Young 1972). It is a strong diel vertical migrator, moving from peak day depths of m to above 400 m at night (Roper and Young 1975). This vertical distribution places a large portion of the population in the core of the oxygen minimum layer off southern California during the day (0, levels ml * liter-l: Emery 1960) and above the minimum layer at night. I thank the officers and crew of the RV Agassix for logistical support and the following individuals for equipment, technical assistance, and advice: M. S. Gordon, J. J. Childrcss, L. Quetin, and J. Torres. M. S. Gordon and R. Young critically reviewed the manuscript. Methods The squid were captured in a 3-m2 Tucker-type midwater trawl in San Clemente Basin (32 30 N, 118 W) and Santa Catalina Basin (33 10 N, 119 3O W) from RV Agassix in September All animals were placed immediately in refrigerated seawater baths at 5 C and kept in these baths until used, usually for no more than 48 h. All experiments were conducted at sea. The pressure vessels (respirometers), the system for generating pressure, and the device used to stir the interior of the vessels are described elsewhere (Belman
2 736 Belman ET F f (12) a =T a m E N (12) (3) 00 E E Y :: 0, I 1 I I PRESSURE - ATMOSPHERES Fig. 1. Effects of hydrostatic pressure on oxygen consumption rates at 5 C in Histioteuthis heteropsis. Means of (n) values &SE and 95% confidence intervals indicated. and Gordon 1978). Individual rates of oxygen consumption were determined from strip-chart records of the decline in oxygen concentration in the sealed pressure vessels. Experimental seawater was taken from the surface in the region where the squid were captured and was collected, filtered (to 100 CL), and stored in an all-plastic system designed for this purpose. Before each experiment, 25 mg. liter-l of streptomycin was added to the water to inhibit microbial growth. Experimental protocol was as follows. Squid were left in the refrigerated seawater bath at 5 C for at least 8 h. They were then gently introduced into the pressure vessels, one squid per vessel. Each squid was given at least 4 h to recover from the shock of handling. During this period air-saturated seawater was added to the pressure vessels to maintain high oxygen levels and temperature was held at 5 + O.l C. The pressure vessels were then sealed and rates of oxygen consumption (V O,) determined as follows: 1 h at 1 atm; 40 min at 68 atm; 40 min at 1 atm; 40 min at 68 aim; 40 min at 1 atm. Five squid were subjected to 34-atm pressure for 40 min following the first return to 1 atm. Three of these five squid were subjected to 136 atm just before the end of the experiment. Each test sequence, including initial handling, lasted no more than 5 h. The oxygen concentra- OXYGEN CONCENTRATION Fig. 2. Effects of oxygen concentration at 68 atm and 5 C on oxygen consumption rates in Histioteuthis heteropsis. n = 5. Means -+SE indicated. tions in the pressure vessels during experiments never fell below 1.5 ml. liter-. Five squid not previously subjected to pressure change were allowed to deplete the oxygen in the pressure vessel to unmeasurably low levels at 68 atm to test the effects of extreme low oxygen on V 02. Three of these squid were allowed to remain in the pressure vessels for 1 h after the oxygen was depleted, to test anaerobic survival. The individual squid were removed from the pressure vessels after each experiment sequence. Their volume was measured by displacement in seawater and they were then frozen. Wet weights were determined in the shore laboratory after defrosting and blotting each squid with paper toweling for 1 min. Weightspecific oxygen consumption rates were calculated on the basis of these wet weights. Since considerable experience has shown no measurable oxygen consumption attributable to microbial contamination at 5 C in the presence of streptomycin, no control determinations were conducted. Results The average V 02 for each 40-min exposure period at each different pressure
3 Pressure effects on respiration 737 was combined for all squid tested. The mean V 02 was then plotted as a function of the test pressure (Fig. 1). It is apparent that increasing hydrostatic pressure (1-136 atm) has no significant effect on V Oe (P < 0.5;f-test). If the mean V Oe at 68 atm (0.030 liter OZ. mg-. h-l) and the V OZ at 1 atm (0.023 liter OZ. mg- * h-l) are compared alone, there is also no significant pressure effect (P s 0.5; f-test). The V OZ of H. heteropsis as a function of available oxygen was examined at 68 atm only. The response above 0.5 ml 02*liter-* indicated that the squid is a good metabolic regulator (Fig. 2). Below 0.5 ml Oz*liter- the V Oe declines more or less as a function of available oxygen. The three squid exposed to anoxic conditions for 1 h were alive after this period and, while initially quiescent, they became active after 5-7 min in freshly aerated seawater. As all squid used were close to the same size (mean: 4.25 g; range: g wet wt), no regression of oxygen consumption rate on body weig -1 It was calculated. Discussion The lack of an effect of I iydrostatic pressure on metabolic rate over the range of pressures (and beyond) to which H. heteropsis is exposed in the open ocean is similar to the observations of Teal and Carey (1967) on epipelagic, vertically migrating euphausiids. It is also similar to data obtained by Pearcy and Small (1968) for several vertically migrating crustaceans, by Smith and Teal (1973) for three species of vertically migrating thecosomatous pteropods, and by Quetin and Childress (1976) for a migratory galetheid crab. The insensitivity to pressure seen at the higher pressures used here (68 and 136 atm) is somewhat surprising since H. heteropsis has a vertical range more typical of deep migrators like the crustaceans examined by Teal (1971), in which a graded response to high pressure was observed. However the crustaceans examined by Teal are not exposed to oxy- gen minimum conditions at day depths, and a different overall pattern of metabolic response to pressure and temperature changes during vertical migration might be expected. The vertically migrating copepod Gaussia princeps has a diel vertical range similar to that of H. heteropsis. Hydrostatic pressure has significant effects on metabolic rate in G. princeps even at pressures as low as 28 atm. Childress (1977) examined these pressure effects at three temperatures and showed that at the higher pressures and lower temperatures characteristic of day depths this species had a significantly lower metabolic rate than at night depths. This is of considerable adaptative advantage since G. princeps stays in the core of the oxygen minimum layer during the day and must rely in part on anaerobic metabolism for its total energy needs. For H. het- eropsis the absence of elevated metabolic rates due to pressure may well combine with a depressing effect of lowered temperature to produce a similar pattern, Limited shiptime and specimen availability prevented any study of metabolic effects of temperature in H. heteropsis. The rates of oxygen consumption reported here for H. heteropsis are the first measurements of this sort for open ocean pelagic squid. No really comparable data on other squid (small respirometers, low temperatures) are available. Oxygen consumption rates at 5 C and at any pressure normally encountered are similar in H. heteropsis to rates of oxygen consumption measured under similar conditions in a number of midwater crus- taceans (Childress 1975). If the criterion of Childress (1975) for the minimum depth of occurrence (MDO) of pelagic species is applied to II. heteropsis, an average 5-g specimen has a MD0 of about 50 m. The predictive formula of Childress (1975) relating oxygen con- sumption rate (V 02) to MD0 (R = 0.695X f0.05; R, liter Oe*mg-l; X, m), suggests that H. heteropsis has a some- what lower rate than expected (predicted R = liter 02.rng-l* h-l). This predictive equation may not apply to ceph-
4 Belman alopod or other noncrustacean organisms. The respiratory rates of epipelagic pteropods reported by Smith and Teal (1973) when examined as a function of MD0 do, however, agree with the equation of Childress. Another possible explanation for the difference between observed and predicted metabolic rates is that using the MD0 concept for strong vertical migrators is valid only if the MD0 is adjusted in some way to partially reflect the difference between day and night depths. If the MD0 for H. heteropsis is taken as the average peak concentration depth of both the day and night depths (400 m), the predicted rate fits the observed rate relatively closely. However, if this criterion is applied to the vertically migrating caridian species examined by Teal (1971), the predicted rates at night depths are more closely related to the observed rates than are predicted rates at the average of night and day depths. The shrimp Systellapsis debilis, for example, has a predicted rate at a MD0 of 105 m (night) of liter Oz. mg-r* h-l and an observed rate at 20 C and 1 atm pressure of about At an average MD0 of 400 m the predicted rate is liter 0,. mg-l. h-l. The species examined by Teal (1971) occur at substantially higher temperatures throughout their depth ranges than do those examined by Childress (1975) and the squid examined here. The absence of an oxygen minimum at daytime depths also presents the species examined by Teal with a basically different set of environmental conditions. Further examination of the rates of oxygen consumption of strong vertical migrators living in different environments may indicate the necessity of modifying the MD0 concept for these forms. Doing this would have the advantage of avoiding the lumping together of strong migrators with nonmigratory surface-living species, and would also prevent any distortion inherent in discussing the respiratory rates of species at day depths which are unrelated to food supplies at night depths. At daytime depths, H. heteropsis is exposed to oxygen levels of around ml - liter-l (Emery 1960). My experimen- tal results suggest that this species cannot obtain sufficient oxygen at these concentrations for its metabolic demand at 5 C, and it is probable that anaerobiosis is important to this species at day depths. Childress (1975) suggested that many mcsopelagic species resident in the oxygen minimum layer off California can support their energy demand aerobically, while other species, like the copepod G. princeps, apparently cannot and must rely at least in part on anaerobiosis. Like G. princeps, H. heteropsis could burn off oxygen debts accumulated in the oxygen minimum layer during migrations into shallow, more oxygen-rich, waters at night. An alternative hypothesis is that II. heteropsis becomes quite lethargic at day depths thereby lowering its total oxygen demand to meet the limited supply. Such a strategy has been suggested for other migratory species (Gordon et al. 1976; Childress 1977), but no direct supporting evidence has yet been presented. Even though H. heteropsis can quite often be captured alive and in apparently healthy condition it will prove difficult to examine in great detail the physiological mechanisms involved in response to pressure changes or lowered ambient oxygen levels. The reason for this is that at present mesopelagic squid do not sur- vive well for more than 4 days under laboratory conditions. Mortality probably cannot be attributed to pressure effects (this study), nor does temperature appear to be a significant factor (R. Young pers. comm.). Mechanical damage during capture and in aquaria (even in large capacity systems) probably is the most serious problem. The development of suitable maintenance and capture systems may therefore be necessary before long term studies of open ocean squid such as H. heteropsis will be feasible. References BELMAN, B. W., AND M. S. GORDON Comparative studies on the metabolism of shallowwater and deep-sea fishes. 5. The effects of temperature and hydrostatic pressure on OXY-
5 Pressure effects on respiration 739 gen consumption in the mesopclagic zoarcid, Melanostigma pammelas. Mar. Biol. in press, CHILDRESS, J. J The respiratory rates of midwater crustaceans as a function of depth of occurrence and relation to the oxygen minimum layer off southern California. Comp. Biothem. Physiol. 50: The effects of pressure, temperature and oxygen on the oxygen consmnption rate of the midwatcr copepod Gaussia princeps. Mar. Biol. 39: EMERY, K The sea off southern CaIifornia. Wiley. GORDON, M. S., B. W. BELMAN,AND P. II. CHOW Comparative studies on the metabolism of shaliow-water and deep-sea fishes. 4. Patterns of aerobic metabolism in the mesonelafzic fangtooth fish Anoplogaster cornuta. Mcr. BIG< 35: MEEK, R. P., AND J. J. CIIILDRESS Respiration and the effect of pressure in the mesopelagic fish Anoplogaster cornuta (Beryciformes). Deep-Sea Res. 20: PEARCY, W. G., AND L. F. SMALL Effects of pressure on the respiration of vertically migrating crustaceans. J. Fish. Res. Bd. Can. 25: 131 l QUETIN, L. B., AND J.J. CHILDRESS Respiratory adaptations of Pleuroncodes planipes Stimpson to its environment off Baja California. Mar. Biol. 38: ROPER, F. E., AND R. E. YOUNC Vertical distribution of pelagic cephalopods. Smithson. Contrib. Zool. 209, p. l-51. SMITH, K. L., AND R. R. HESSLER Respiration of benthopelagic fishes: In situ measurements at 1230 meters. Science 184: , AND J. M. TEAL Temperature and pressure effects on respiration of thecosomatous pteropods. Deep-Sea Res. 20: TEAL, J. M Pressure effects on the respiration of vertically migrating decapod crustacea. Am. Zool. 11: AND F. G. CAREY Effects of pressure an d temperature on the respiration of euphausiids. Deep-Sea Res. 14: YOUNG, R. E The systematics and aeral distribution of the cephalopods from the seas off southern California. Smithson. Contrib. Zool. 97, 1~. l-159. Submitted: 21 March 1977 Accepted: 29 November 1977
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