The influence of temperature acclimation upon the metabolic rate of the purple sea urchin, Strongylocentrotus purpuratus: Alternate interpretations

Camp. Biochem. Physiol., 1973, Vol. 45A,pp. 677 to 681. Pergamon Press. Printed in Great Britain

SHORT COMMUNICATION THE INFLUENCE OF TEMPERATURE ACCLIMATION UPON THE METABOLIC RATE OF THE PURPLE SEA URCHIN, STRONGYLOCENTROTUS PURPURATUS: ALTERNATE INTERPRETATIONS RICHARD

J. ULBRICHT

Department of Zoology, Oregon State University, Corvallis, Oregon 97331, and Marine Science Center, Newport, Oregon 97365, U.S.A. (Received

15 September

1972)

Abstract-l. The purple sea urchin, Strongylocentrotus purpuratus, was acclimated at 9 and 18°C for 30 days. 2. Following acclimation, metabolic rate-temperature relationships were determined. The effect of acclimation varies, dependent upon the metabolic rate expression used. 3. Advantages of dry weight-standardized oxygen consumption rates are discussed. INTRODUCTION

NUMEROUSstudies dealing with the effect of temperature acclimation upon poikilotherm rate functions are reviewed by Bullock (1955), Fry (1958), Precht (1958, 1968) and Prosser (1964,1967). Although various patterns of response are possible, cold-acclimated organisms are generally described as having higher rates, along with lower temperature coefficients, than warm-acclimated forms at the same test temperature. Following temperature acclimation of Strongylocentrotzls purpuratus, cold-acclimated urchins possessed higher oxygen consumption rates than did warmacclimated forms (Farmanfarmaian & Giese, 1963). The degree to which this acclimation effect manifests itself in the respiratory metabolism of Oregon urchins (approx 44.5” N) is of interest.

MATERIALS

AND METHODS

Purple urchins, S. purpuratus, were collected over a narrow latitudinal range along the central Oregon coast and maintained in aerated sea water aquaria at the Marine Science Center. Ten urchins were acclimated for 30 days at 9°C while six were acclimated at 18°C. The term acclimation is used as defined by Prosser & Brown (1961). Therefore, all other factors were constant. Urchins were fed macroscopic algae to satiety during the first 2 weeks of acclimation. No effort was made to feed them throughout the remainder of the 30 days. Aquarium water was changed as necessary. 677

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RICHARDJ. ULBRICHT

Following acclimation, oxygen consumption by intact urchins was determined by closed volume respirometry as detailed by Ulbricht & Pritchard (1972). Urchin size ranged from 17.2 to 153*7 g (wet) and 0.53 to 7.23 g (ash-free dry). Ash-free dry weight was assumed to be the difference between total dry weight and the ash recovered after 24 hr at 500°C. Presumably, this weight represents the “organic” component. Oxygen consumption measurements were made at 6, 9, 12, 15, 18, 21 and 24°C (see Ulbricht & Pritchard, 1972, for the protocol). Rates are expressed as ~1 of oxygen consumed per g per hr &l 0,/g wet per hr for wet weights and ~1 OS/g dry per hr for ash-free dry weights).

RESULTS AND DISCUSSION

The inverse relationship between metabolic rate and size of organism is reviewed by Zeuthen (1953) and Hemmingsen (1960). Urchin rates were corrected to 91.2 g (wet) and 4.06 g (ash-f ree dry), the approximate mean weights, through linear regression analysis of log rate on log size. Rate-temperature relationships (R-T curves) for temperature-acclimated S. purpuratus are depicted in Figs. 1 and 2 (wet and ash-free dry weight-standardized rates, respectively). Identical data excluding the weight values were used to determine these R-T curves. Interval estimates for the means were determined as outlined by Ulbricht & Pritchard (1972). Qi,, values are presented in Table 1. purple R-T curves of temperature-acclimated Wet weight-standardized urchins provide some indication of partial compensation (type 3, Precht, 1958, 1968). At test temperatures of 21 and 24°C differences are significant at the

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9

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FIG. 1. Oxygen consumption rate-temperature curves for temperature-acclimated S. purpuratus (91.2 g wet). (a), 9°Cacclimated urchins; (A), 18°Cacclimated urchins; vertical bars indicate 95 per cent confidence limits.

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RATE OF THE PURPLE SEA URCHIN

679

95 per cent confidence level (Fig. 1). This type of compensation was observed to a greater extent with temperature-acclimated purple urchins collected from the central California coast (Farmanfarmaian & Giese, 1963). On the other hand, ash-free dry weight-standardized R-T curves provide little indication of partial compensation (Fig. 2). In fact, inverse compensation (type 5, Precht, 1958, 1968) is suggested at test temperatures of 12 and 15°C.

6

9

12

15 oc

21

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FIG. 2. Oxygen consumption rate-temperature

curves for temperature-acclimated S. purpurutus (4.06 g ash-free dry). (a), 9%acclimated urchins; (A), 18% acclimated urchins; vertical bars indicate 9.5 per cent confidence limits.

In spite of the disparate interpretations-i.e. partial vs. inverse compensationtemperature coefficients of both rate expressions are in good agreement with each other (Table 1). For example, Qi,, values of urchins acclimated at 9°C are lower between 6 and 12°C than those of urchins acclimated at 18°C. Conversely, Qlo values of warm-acclimated urchins are lower between 12 and 21°C than those of cold-acclimated forms. Lower Q10 values for cold-acclimated urchins between 21 and 24°C possibly reflect a decreasing well-being of these forms within this range (see Bullock, 1955). Greater rate-temperature independence occurs at test temperatures close to temperatures of acclimation. Urchins were not fed following 2 weeks of acclimation in order to minimize the effect of nutritional state on metabolic rate (see Farmanfarmaian, 1966). Possibly a postabsorptive condition was achieved before concluding the acclimation period. Tissue resorption may have followed.

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RICHARDJ. ULBRICHT

TABLE I-Qro

VALUES FOR OXYGENCONSUMPTION RATE-TEMPERATURE RELATIONSHIPS OF TEMPERATURE-ACCLIMATED S. purpuratus Wet weight*

Temperature range 6-9 9-12 12-15 IS-18 18-21 21-24

Coldacclimated 3.22 2.28 2.86 4.04 2.65 1.64

Ash-free dry weight?

Warmacclimated 6.83 3.61 1.94 1.99 1.89 2.10

Coldacclimated 4.04 2.28 2.52 4.31 2.72 I.55

Warmacclimated 7.50 5.98 2.28 1.74 I.79 I.89

* Coefficients of rates standardized to a 91.2 g (wet) urchin. t Coefficients of rates standardized to a 4.06 g (ash-free dry) urchin.

In an adjunct study, purple urchins acclimated as above (eleven urchins at each temperature) were subsequently partitioned into various body componentsbody wall including the lantern apparatus, gonads and the remaining internal, nongerminal tissues (hereafter called “gut”). Ash-free dry weight determinations were made. The only significant difference in component weights between acclimation groups lay with the gut. Gut weight of cold-acclimated urchins was 0.37 g (14.1 per cent of total ash-free dry weight) compared to the 0.26 g (11.1 per cent of the total) of warm-acclimated forms (Ulbricht, unpublished). Both differences between means, 0.11 g and 3-O per cent, are significant at the 95 per cent confidence level. The gut mean weight difference may reflect greater metabolic demands for maintenance level activity for warm-acclimated forms. Rate-temperature and weight partition data came from separate groups of temperature-acclimated urchins. Urchins used in the rate study were collected in summer, whereas those used for partitioning were spring forms. Therefore, interpretations combining these studies must be tentative. Nevertheless, urchins in both studies were treated similarly over a 30 day acclimation period. One might reasonably expect seasonal differences in metabolic rate and component weight to be reduced following acclimation. Dry weight-standardized rates were determined in order to reduce errors while measuring urchin size. Interpretation of the present study discloses a second advantage. Perivisceral fluid mass would be included in the determination of wet but not dry weight-standardized rates. It comprises from 18.7 to 34.2 per cent of the total wet weight of a 15-26 g urchin (Giese et al., 1966). However, oxygen consumption by this component in a&o is remarkably low due to a negligible oxygen consumption rate-l.1 ~10,/g per hr (Giese et al., 1966). Oxygen consumption by the fluid may be different with intact urchins. Nevertheless, the effect of including fluid weight would be to markedly decrease whole urchin metabolic rate.

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It is tempting to suggest that during acclimation more gut resorption occurred with warm-acclimated urchins than with cold-acclimated. Presumably, perivisceral fluid replaced the resorbed tissue. This sequence may underlie the paradoxical interpretations involving the R-T curves. There is a need to evaluate all component weights when dealing with whole animal “wet weight” metabolic rates. If a component with characteristics of perivisceral fluid-large fraction of the total wet weight and nearly negligible contribution to overall metabolism-is sensitive to variation in the study, an alternate rate expression may be necessary. REFERENCES BULLOCKT. H. (1955) Compensation for temperature in the metabolism and activity of poikilotherms. Biol. Rev. 30, 311-342. FARMANFARMAIAN A. (1966) The respiratory physiology of echinoderms. In Physiology of Echinodermata (Edited by BOOLOOTIAN R. A.), pp. 245-265. Interscience, New York. FARMANFARMAIAN A. & GIESE A. C. (1963) Thermal tolerance and acclimation in the western purple sea urchin Strongylocentrotus purpuratus. Physiol. Zoiil. 36, 237-243. FRY F. E. J. (1958) Temperature compensation. A. Rev. Physiol. 20, 207-224. GIESE A. C., FARMANFARMAIAN A., HILDEN S. & DOEZEMAP. (1966) Respiration during the reproductive cycle in the sea urchin, Strongylocentrotus purpuratus. Biol. Bull. mar. biol. Lab., Woods Hole 130, 192-201. HEMMINGSENA. M. (1960) Energy metabolism as related to body size and respiratory surfaces, and its evolution. Rep. Steno meml Hosp. 9 (part 2), l-110. PRECHTH. (1958) Concepts of the temperature adaptation of unchanging reaction systems of cold-blooded animals. In Physiological Adaptation (Edited by PROSSERC. L.), pp. 50-78. American Physiological Society, Washington, D.C. PRECHTH. (1968) Der Einfluss “normaler” Temperaturen auf Lebensprozesse bei wechselwarmen Tieren unter Ausschluss der Wachstums- und Entwicklungsprozesse. Helgol&der wiss. Meeresunters. 18, 487-548. PROSSERC. L. (1964) Perspectives of adaptation: theoretical aspects. In Handbook of Physiology, Sect. 4, Adaptation to the Environment (Edited by DILL D. B., ADOLPH E. F. & WILBER C. G.), pp. 11-25. American Physiological Society, Washington, D.C. PROSSERC. L. (1967) Molecular mechanisms of temperature adaptation in relation to speciation. In Molecular Mechanisms of Temperature Adaptation (Edited by PROSSERC. L.), pp. 351-376. A.A.A.S., Washington, D.C. PROSSERC. L. & BROWN F. A., JR. (1961) Comparative Animal Physiology, 2nd Edition. p. 688. Saunders, Philadelphia. ULBRICHT R. J. & PRITCHARDA. W. (1972) Effect of temperature on the metabolic rate of sea urchins. Biol. Bull. mar. biol. Lab., Woods Hole 142, 178-185. ZEUTHENE. (1953) Oxygen uptake as related to body size in organisms. Q. Rev. Biol. 28, 1-12. Key Word Index-Temperature acclimation; purpuratus; metabolic rate; oxygen consumption.

purple sea urchin;

Strongylocentrotus