The effect of body size and temperature on the respiration of Polinices duplicatus

Camp. Biochem. Physiol., 1973, Vol. 44A, pp. 1185 to 1197. Perganon Press. Printed in Great Britain

THE EFFECT OF BODY SIZE AND TEMPERATURE ON THE RESPIRATION OF POLINICES DUPLICATUS JUDITH Department

D. HUEBNER*

of Zoology, University of Massachusetts, Amherst, Massachusetts 01002

(Received 11 July 1972) Abstract-1. Although variable, respiration is proportional to the 0.536 power of wet weight for Polinices duplicatus at all temperatures and seasons tested. 2. QrO is inversely proportional to size between 15 and 30°C and directly porportional to size between 5 and 10°C. 3. Level of metabolism is directly proportional to temperature. 4. Crawling activity is 35 per cent less between 5 and 10°C than between 15 and 30°C. 5. There is no evidence of seasonal acclimation of respiration in P. duplicatus. 6. Possible adaptive significance and physiological mechanisms for patterns of respiration found, and the possibility of a metabolic “switch” are discussed.

INTRODUCTION

THE TEMPERATE intertidal zone is among the most rigorous habitats with extensive and rapid changes in temperature (Johnson, 1965 ; Green & Hobson, 1970) both daily and seasonally, alternations of exposure and inundation, and rapid depletion of oxygen with depth in the sediment (Brafield, 1965 ; Jansson, 1967). For these reasons, only animals capable of physiological compensation for such environmental changes live in this habitat. Polities duplicatus is a carnivorous prosobranch from the intertidal zone along the east coast of the United States as far north as Cape Anne, Massachusetts. Respiration of individuals from a northern population was studied in order to (1) investigate respiratory responses of an intertidal predator to changes in temperature and season and (2) collect sufficient respiratory data for the construction of energy budgets for the species which will be the subject of another communication. In addition to temperature and season, animal size influences respiration in animals. The expression M = aWb (M = oxygen consumption, W = body weight and a and b are constants) defines the relationship between metabolism and body size. A logarithmic plot of M and W results in a straight line whose slope b is the coefficient of respiration. Although Brody (1945) and Zeuthen (1953) found a respiration coefficient (b) of 0.67 applicable to homeotherms, suggesting that respiration is dependent on the surface : volume relationship, Hemmingsen (1960) * Present Canada.

address:

c/o Institute

of Parasitology, 1185

Macdonald

College 800,

Quebec,

1186

JUDITH D. HIJEBNER

concluded that 0.75 + 0.015 was the usual value for poikilotherms. Overall, respiration coefficients appear variable, even among closely related species (Barnes & Barnes, 1969) but most fall between 0.6 and 1.0. Metabolism increases with temperature as well as with body size (Krogh, 1941; Bullock, 1955). In addition, temperature often alters the relationship between weight and respiration (b-values) resulting in size-dependence of Qlo measured over the same temperature range. (Q1s is the change in respiration for a 10°C change in temperature.) As temperature increases, Qlo for various invertebrates decreases (Akerlund, 1969), increases (Rao & Bullock, 1954) or remains unchanged (Pamatmat, 1969), although an inverse relationship between Qr,, and temperature is most common (Precht, 1958). The relationships between respiration and body size and temperature are also influenced by an animal’s activity at the time of testing (Newell & Northcroft, 1967; Newell, 1969) and by acclimatization to seasonal changes in field temperatures. Simultaneous measurements of activity and respiration of invertebrates are, however, often imprecise and diflicult to obtain. Moreover, variations in the physiological state of the animals (e.g. reproductive, nutritional) at different times of the year are often neglected in investigations of seasonal temperature acclimatization. MATERIALS

AND METHODS

Collection and mahenance of maa% in the laboratory Snails were collected at approximately monthly intervals throughout the yesfr (1970-71) near Indian Trail Landing, B-table Harbor, Maaoachueetta. The animals were kept without food for 2-14 days in 3-4 1. of aerated artificial sea water in 7-1. plastic aquaria. Aquaria were kept in the dark or in dim light at the desired holding temperature. Table 1 lista holding and test temperatures, which were normally those appropriate for the time of TABLE l--SUMMARY

OF HOLDING AND EXPERIMENTAL TEMPER.4~ WPBRIMENTS

Collection date

Holding temperature (“C) (?r l*O”C)

28 June 1970 11 July 1970 24 July 1970 8 Aug. 1970 28 Sept. 1970 7 Nov. 1970 9 Dec. 1970 21 Feb. 1971 8 Mar. 1971 22 Mar. 1971 24 Apr. 1971 22 May 1971 6 June 1971 25 June 1971

20.0 20.0 20.0 20.0 15.0 5.0 5.0 5.0 5.0 5.0 15.0 15.0 20.0 20.0

USED IN RESPIRATION

Test temperature (“C) ( & 0*.5”C) 20.0 25.0, 20.0 25.0, 15.0, 5.0, 5.0, 5.0, 15.0, 5.0, 15.0, 15.0, 5.0, 20.0,

30.0 30.0 20.0 10.0 10.0 10.0 20.0 10.0 20.0 20.0 10.0 25.0, 30.0

RESPIRATION

OF

POLINICES

DUPLICATUS

1187

collection (based on Green & Hobson, 1970, and records of the Woods Hole Oceanographic Institution). Additional determinations in March and June 1971, were performed at temperatures approximating those of other seasons. Apparatus and measurements The bottom of a 2.8-l. Fembach flask was covered with a thin layer of clean gravel and filled with filtered, aerated artificial sea water at the desired temperature. After a single snail was placed inside, the flask was closed with a rubber stopper through which a Clark type polarographic oxygen electrode (YSI SlA, Yellow Springs Instrument Co., Yellow Springs, Ohio) was inserted. The flask was kept in a constant temperature bath except when measurements of oxygen concentration were being made. During the readings, the water was circulated gently by a magnetic flea. Measurements were made each hour (except for the two experiments done at off-season temperatures for which measurements were made only at the start and finish of the run) for 5 hr, or until (as happened at high temperatures) the oxygen concentration fell below 1.5 ppm. At the beginning and end of each series of experiments, the electrode was calibrated in air; dissolved oxygen was also measured by the Winkler method at these times (American Public Health Association, 1965). Readings from control flasks containing only artificial sea water and gravel showed no oxygen consumption, indicating that only the following small corrections for changes in electrode calibration during the experiments were needed: -0.25 ppm at 5°C; -0.20 ppm at 10°C; -0.05 ppm at 15 and 20°C; 0.10 ppm at 30°C. Ten snails from each collection were used at each temperature. When respiration of snails from one collection was determined at two or three temperatures, temperatures were alternated daily until the series of experiments was completed thereby assuring that animals tested at various temperatures were exposed to laboratory conditions for similar lengths of time. If the experimental temperature differed from the holding temperature, the snail was allowed 1 hr at the test temperature in a separate container before measurements were begun. In all experiments the snail’s activity was observed and recorded. A snail was considered active if it was crawling at the time of the reading, inactive if it was motionless or withdrawn into its shell and was not classified if it was on its back with its foot partially or entirely expanded. At the end of each experiment, snails were measured, and fresh weights were obtained after removal of the shell and operculum. Dry weights were recorded after 72 hr at 60°C and ash weights after 24 hr at 600-65O”C. Ash-free dry weights were calculated by difference. Manual calculations were done with a Wang programmable calculator (Wang, Model 380). Regression analyses and analyses of covariance were done with a CDC-3600 computer using UCLA Biomed series programs BMDOlR and BMD03R. Comparisons of slopes and elevations of regression equations were performed according to Snedecor & Co&ran (1967). When a common slope was applied to equations, new intercepts were derived from the means of the data. RESULTS

Following the convention set by Zeuthen (1953), oxygen uptake/hr per animal will be referred to as metabolism or respiration and oxygen uptake/hr per g as metabolic or respiration rate or weight-specific metabolism. Since the correlation (I) between oxygen uptake and weight was consistently higher with shell-less wet weight than with ash-free dry weight, all calculations are based on wet weights. This should be taken into account when comparisons are made with the results of others, since regression coefficients change when different measures of weight are

1188

JUDITH D. HLBNER

used. To facilitate comparisons, calculations were made for a “standard” animal of 5 g wet weight. This choice was based upon the mean weight of all snails tested (5.25 g). Figure 1 s ummarizes the relation between respiration and fresh weight of P. duplicatw at different temperatures and seasons. There are no significant differences among b-values for the temperatures and seasons tested (analvsis of covariance, >-test, 5 per cent level), so all data (Table 2) were pooled to

FIG. 1. Respiration of P. duplicatus at temperatures from 5 to 30°C using common respiration coefficient of 0.536. Figure Sa--5°C. b-10°C. ~-15°C. d-20°C. -25°C. f-30°C. Dates of collection are designated as follows: A = Feb. 1971, B = Mar. 1971, C = Apr. 1971, D = May 1971, E = June 1970, E’ = June 1971, F = July 1970, G = Aug. 1970, H = Sept. 1970, J = Nov. 1970, K = Dec. 1970, * = All tests at the designated temperature.

obtain a common respiration coefficient of b = 0.536. Since slopes for all March tests (S-2O”C), 5°C in June and December, and 30°C in June 1971 did not differ statistically from either zero or the common slope, the common respiration coefficient was applied to them as well. Respiration increased directly with temperature to a maximum at 25”C, as illustrated for a standard (5 g) animal (Fig. 2) ; t = 0439 when the 30°C tests are excluded. The Y-intercept (u-value), another indication of metabolism, was also positively correlated with temperature; Y= 0.96 when means of u-values for the same temperature, adjusted to b = 0.536 are used (Fig. 3). The reduced activity of the snails at low temperatures may be partly responsible for the relationship:

RESPIRATION OF POLINICES

1189

DUPLICATUS

rF-G

IO00 -

E-F

l%O-

/ E’ H

600& \

4 D/

0" 400r zi

C/

200-

OL

I

1

5

IO

I

15

Tempemture,

I

I

I

20

25

30

C

FIG. 2. The respiration of a standard (5 g) P. duplicates at various temperatures and seasons using the common respiration coefficient of 0536. Symbols for collection dates as in Fig. 1.

262.52,4f

2.3 -

> b P

2.2-

8

a

2.1-

PO1.9I.8 0

5

IO

15

20

Temperature,

25

30

C

FIG. 3. Respiration level (u-value) of P. duplicatus for temperatures of S-25°C using common respiration coefficient of 0536; a = 1*72+0*03 (“C).

snails were active at 88 per cent of the readings made at 15-30°C but were active at only 52 per cent of the readings at 5 and 10°C. Animals were inactive at 3 and 34 per cent of the readings at 15-30 and 5-lO”C, respectively. Since analysis of covariance indicated that a-values of the following samples were not significantly different at the 5 per cent level, they were grouped: all 5°C tests, all 10°C tests, all winter tests at 5 and lO”C, all 20°C tests except March, all 25°C tests, all 30°C tests (see Table 2).

1190

JUDITHD. HUZBNBR

TABLE 2-TERMS

OF REGRESSION EQUATIONS:

TIONSHIP BETWEEN OXYGEN CONSUMPTION

Date and temperature PC) 5 5 5 5 5 10 10 10 10 10 15 15 15 15 20 20 20 20 20 20 20 25 25 25 30 30 30 5 10 15 20

J”” k

A, B,

J”” I;, A, B, I-5 B,

c

D, E,

E’, F, H, B,

c,

D, E’s F, G, E’, F, G,

All All C, D All

All (exc;$ W All 30 All E’

log

( y)

Y = U+b

lOg x,

DESCRIBING

AND WET WEIGHT (x)

OF P.

Y

(adj:ed to b = 0.536)

0.329 f 0.218 0.409 f0.116 0.322 f 0.462 0.391 f 0.103 0.695 f 0440 0.604 f 0.138 0.514 f 0.083 0.995 f 0.168 0.361 f 0.103 0.432 f 0.533 0.735 f 0.121 0.326 f 0.331 0.887 f 0.236 0468 f 0.073 0.865 f 0.220 0.663 f 0.190 0.621 f OW8 0.722 f 0.067 0.278 f 0.258 0.414 f 0.065 0.348 f 0.079 0.615 f 0173 0.778 f 0.096 0.479 f 0.079 0.312 f0.153 0~56Of0~112 0406 f 0.114 0400 f 0.087 0.527 it 0.078 0.541 kO.116 o-531 f 0.050

0.49 0.70 0.26 0.80 0.58 0.86 0.91 0.91 0.64 0.31 0.92 0.35 0.82 0.92 0.83 0.80 0.98 0.97 0.38 0.93 0.86 0.80 0.95 0.92 0.61 0.88 0.80 0.56 0.70 0.58 0.81

1.91 1.82 1.84 1.92 1.81 2.01 2.09 1.98 1.96 1.95 2.42 2,03 2.20 2.31 2.35 2.42 2.50 2.53 2.14 2.35 2.44 2.53 2.53 2.66 2.48 2.60 2.66 1.86 2.00 2.25 2.43

0.594 f 0.072 0.373 f 0.066 0480 f 0.093

0.84 0.74 0.72

2.57 2.56 2.48

N

a-value

b f SE

10 10 10 11 10 10 10 10 10 10 10 8 10 10 10 10 10 10 9 10 10 10 10 10 10 10 10 49 50 20 60

2.01 1.89 1.97 1.99 1.72 1.97 2.10 1.74 2.06 2.01 2.28 2.15 1.96 2.35 2.11 2.34 2.44 2.41 2.27 2.41 2.53 2.48 2.37 2.69 2.65 2.54 2.70 1.94 2.00 2.17 2.44

30 30 30

2.53 2.66 2.36

THE RELA-

du~licuiur

Collection dates are designated an follows: A = Feb. 1971, B = Mar. 1971, C = Apr. 1971, D = May 1971, E = June 1970, E’ = June 1971, F = July 1970, G = Aug. 1970, H = Sept. 1970, J = Nov. 1970, K = Dec. 1970.

QIO reflects respiratory response to changes in temperature and varies with both size and temperature for P. duplziutus. Between 15 and 3O”C, Qlo is inversely proportional to animal size, whereas between 5 and 10°C (except in March), it is directly proportional to size (Fig. 4). This relationship of Qlo to size is eliminated

IWSPIRATION

OF POLINICES

when all equations are adjusted to b = 0.536. Q10 is temperature, with no clear relationship to temperature no broad temperature range over which QIO remains values rarely exceed 2.0 except at low temperatures ( < IOOk

1191

DUPLICATUS

quite variable at any given (Fig. 5). Although there is constant for P. duplicatus, 1OT). I If Q,, is considered c)

(b)

5.0 -

B I.0 r

Wet wt of PohMes,

g

FIG. 4. Relationship between Q10 and wet weight of P. duplicaturat various temperatures and seasons based on original regression equations. Figure 4(a)5-10°C. (b)--1%20°C. (c)-Upper three lines 20-25”C, lower three lines 25-30X!. Symbols for collection dates as in Fig. 1.

4.01 *J 3.0 -

20-

B

I .o-

PG OE’

06’

I

I

I

I

5-10

IO-15

B-20

20-25

Temwmtvre,

I 25-x,

C

FIG. 5. Q,, values for a standard (5 g) P. duplicatusat various seasons and temperatures based on equations using wmmon respiration coefficient of 0.536. Circles used for separate collection dates, crosses ( x ) for PI,, derived from all tests at the given temperature. Symbols for collection dates as Fig. 1.

1192

JUDITHD. HUEBNER

over

the classical temperature interval of lO”C, there is a loss of information (e.g. is lower for 20-30°C than for 20-25°C because respiration shows no further Ql0 increase above 25°C). Both Qi,, and metabolism vary with season as well as temperature and animal size (Figs. 1, 2, 4 and 5). Thus, in the fall when holding and field temperatures (Green & Hobson, 1970) were lower than in summer, respiration at 20°C was higher than in summer. When temperatures were still lower (e.g. in March), however, respiration at 20°C decreased considerably. Though there is a general decrease in Qis throughout the winter and summer and an increase through the spring, trends are not very strong. When animals were tested at temperatures inappropriate for the collection time, the relationship between size and respiration tended to break down (e.g. 5°C in June, 15 and 20°C in March). In part this is due to large variability and general immobility of the snails under these conditions. In addition, respiration appeared to be depressed when animals were tested at unusually high temperatures such as 15 and 20°C in March and 30°C in June. Q1,,, activity level, and to a lesser extent, level of metabolism (u-value) (Paloheimo & Dickie, 1966) all exhibit a discontinuity between 10 and 15°C. Thus, Q usually increases with animal size at 5 and lO”C, but decreases with size at teiperatures 2 15°C (Fig. 4). Activity (as defined in Materials and Methods) decreases by about 35 per cent between 15 and lO”C, but is fairly constant at higher and lower temperatures. In addition, the relationship between u-values and temperature changes somewhat between 10 and 15°C. DISCUSSION

P. duplicatus conform to the expected pattern of increasing respiration and decreasing weight-specific respiration with increasing animal size (Fig. 1; Krogh, 1941; Brody, 1945 ; Rao & Bullock, 1954; Bullock, 1955). Studies of many invertebrates are consistent with Hemmin gsen’s respiration coefficient of 0.75 (e.g. Roberts, 1957a; Berg & Ockelmann, 1959; Davies, 1966; Pamatmat, 1969; Hughes, 1970), but others present quite different values (e.g. Dehnel, 1960; Newell & Northcroft, 1965; Davies & Walkey, 1966; Akerlund, 1969; Rising & Armitage, 1969). For P. duplicatus a common respiration coefficient of 0.536, conforming neither to the range suggested by Hemmingsen (1960) nor Bertalanfiy (1951, 1957), applies to snails from all collections regardless of season and temperature. Davies & Walkey (1966) proposed that such nonconformist respiration coefficients be regarded as “deviation(s) from the phylogenetic b-value of 0*75”, but available data appear to support neither a phylogenetic nor an ecological consistency in respiration coefficients, e.g. the b-value is 0.536 for P. duplicatus, O-52 for the cestode Schistocephalus solidus (Davies & Walkey, 1966) and 0.95 for the prosobranch mollusc Theodoxus fluwiatilus (Berg & Ockelmann, 1959). There is currently no explanation for the various b-values found among poikilotherms, which suggests that a variety of environmental factors and inherent physiological mechanisms (Dehnel & McCaughran, 1964) are responsible for determining the respiration: weight relationships of different species.

RESPIRATION

OF POLINKES

DUPLICATUS

1193

Newell & Northcroft (1967) and Newell (1969) among others have divided metabolism into active and standard phases. The former varies in the predicted manner, directly with temperature, whereas the latter is considered relatively temperature-independent (McFarland & Pickens, 1965 ; Newell, 1966; Halcrow & Boyd, 1967; Sandison, 1967; Newell & Pye, 1970a, b, 1971). This is not true for all animals, however, as shown recently for the dipteran Calliphora erythrocephala (Tribe & Bowler, 1968), the polychaete Diopatra cuprea (Magnum & Sassaman, 1969), the crab Cmcinus and the mollusc Pat&a vulgata (Davies & Tribe, 1969). Whether there are two distinguishable phases of metabolism for P. duplicatus could not be determined in this study, but depressed metabolism at 5 and 10°C may be related to reduced activity at these temperatures. Halcrow & Boyd (1967) state that the influence of temperature on invertebrate metabolism is an expression of change in locomotor activity; the spontaneous activity on which “routine” metabolism is based (Beamish & Mookherjii, 1964) is temperature-dependent (Halcrow & Boyd, 1967). Low respiration and respiration coefficients which do not differ significantly from zero, as well as cessation of feeding (Hanks, 1953), suggest that for P. duplicatus 5°C is near the lower limit of activity and possibly of aerobic respiration. Lewis (1971) obtained similar results for tropical gastropods at 20°C. There is also a levelling off, or decrease in respiration at excessively high temperatures (e.g. 30°C in summer and 20°C in winter) in P. duplicatus and other species (Read, 1962; Newell & Pye, 1970a). The Q10 of invertebrate poikilotherms may vary inversely (Akerlund, 1969; Barnes & Barnes, 1969), directly (Rao & Bullock, 1954; Pickens, 1965; Mason, 1971) or not at all (Roberts, 1957b; Pamatmat, 1969) with animal size. In P. dupzicatus it appears to vary inversely with size between 15 and 3O”C, but (except in February and March) directly with size between 5 and 10°C (Fig. 4) suggesting that large snails are more sensitive to temperature changes when cold, or in winter, and small snails are more affected when warm, or in summer. Many temperate zone poikilotherms (Bullock, 1955 ; Precht, 1958; Beamish, 1964) exhibit an inverse relationship between Qlo and temperature. Other species may exhibit a peak Q10 value at a particular temperature with lower values at both higher and lower temperatures (Read, 1962). Although there is no clear pattern for P. duplicates, QIO values are relatively low, between 1.0 and 2-O for most temperatures, and substantially exceed 2.0 only between 5 and 10°C in November and December (Fig. 5). Such responses to changes in temperature may be beneficial to eurythermal species permitting individuals to preserve a fairly constant metabolism when subjected to rapid fluctuations in temperature such as may occur during a tidal cycle. There may be an especially advantageous energy saving for large animals at high temperatures, reducing somewhat the amount of food they need for maintenance metabolism. The physiological mechanisms responsible for increased Q10 values at low temperatures may enable snails to respond to brief warm spells with increased activity and possibly even feeding. Teal (1957)

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JUDITH D.HUEBNER

suggested that high Qr,, values may be important in the conservation of resources by poikilotherms in winter. Respiration coefhcients, Qis, level of metabolism and activity level of P. duplicutus are all independent of season, although all but respiration coefficients are influenced by temperature. While many species show season-dependent changes in these parameters (Rao & Bullock, 1954; Berg et al., 1958; Newell & Pye, 1970a; Burky, 1971), others, like P. d&pZicutus,do not (&gal, 1956; Barnes ef al., 1963; McFarland & Pickens, 1965 ; Davies, 1967). Newell & Pye (1970a, b) showed that seasonal changes in temperatures of maximal metabolism and low Qi,, values for both active and standard metabolism of intact Litiotina and M’tiruF and cell-free homogenates were directly dependent upon acclimation temperatures. In contrast to the subtidal D. cupreu (Mangum & Sassaman, 1969), in Littoka and ZUytiIus this acclimation process occurs only after several days (Newell & Pye, 1970b), ‘which would make these intertidal molluscs relatively independent of rapid daily fluctuations in temperature. Lack of metabolic changes in P. dupZicatu.s after several days’ acclimation at holding temperatures in the laboratory suggests similar compensatory mechanisms in this species. It is possible, however, that gradual acclimation of snails to unseasonable temperatures was responsible for the high variability during experiments run at such temperatures. The consistent presence of a discontinuity in QiO, activity level, and to a lesser extent, level of metabolism between 10 and 15°C suggests the possibihty of a “metabolic switch” that changes the animal’s respiratory patterns to adapt it to changes in temperature. It appears that temperature is the critical factor triggering the “switch” since animals tested at the same temperature at different seasons responded in the same way. Recent studies (e.g. Hochachka & Somero, 1968; Somero, 1969b; Baldwin, 1971; Somero & Hochachka, 1971) suggest that alterations in isozyme proportions (as well as changes in animal activity) may be responsible for general respiratory responses to temperature, as well as phenomena such as seen between 10 and 15°C and suggested for temperatures below 5°C in P. duplicatus. Temperaturedependent interconversions of isoxymes (Somero, 1969a), favoring the isozyme with the minimal K,,, at the acclimation temperature, could compensate for direct thermal influences on the rates of metabolic processes. Acknowledgements--I wish to thank Drs. D. Craig Edwards, Donald Fairbeim and John L. Roberts for their criticisms of the manuscript and helpful discussions throughout.

REFERENCES AKERLUNDJ. (1969) Oxygen consumption of the ampullariid snail Murisu contumieris L. in relation to body weight and temperature. Oikos 20, 529433. AMERICANPUBLIC HEALTH ASSOCIATION (1965) Standard Methodc for the Examination of Water and Sewage, 12th edn. Am. Publ. Health Assoc., New York. BALDWIN J. (1971) Adaptation of enzymes to temperature: acetylcholinesterases in the central nervous system of fishes. Camp. Biochem. Physiol. 4OB, 181-197.

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DUPLICATVS

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BARNESH. & BARNEYM. (1969) Seasonal changes in acutely determined oxygen consumption and effect of temperature for three common cirripedes, Balanus balanoides (L.), B. balanus (L.) and Chthamalus stellatus (Poli). J. exp. mar. Biol. Ecol. 4, 36-50. BARNESH., BARNESM. & FINLAYSOND. M. (1963) The seasonal changes in body weight, biochemical composition and oxygen uptake of two common boreo-arctic cirripedes, Balanus balanoides and B. balanus. J. mar. Biol. Ass. U.K. 43, 185-211. BEAMISHF. W. H. (1964) Respiration of fishes with special emphasis on standard oxygen consumption-II. Influence of weight and temperature on respiration of several species. Can. J, 2001. 42, 177-188. BEAMISHF. W. H. & MOOKHERJIIP. S. (1964) Respiration of fishes with special emphasis on standard oxygen consumption-I. Influence of weight and temperature on respiraration of goldfish, Carassius auratus L. Can. J. Zool. 42, 161-175. BERG K., LUMBYE J. & OCKELMANNK. W. (1958) Seasonal and experimental variations of the oxygen consumption of the limpet AncylusfEuviatilis (0. F. MULLER). r. exp. Biol. 35,43-73. BERG K. & OCKELMANNK. W. (1959) The respiration of freshwater snails. J. ezp. Biol. 36, 690-708. VON BERTALANFFYL. (1951) Metabolic types and growth types. Am. Nat. 85, 111-117. VONBERTALANFFYL. (1957) Quantitative laws in metabolism and growth. Q. Rev. Biol. 32, 217-231. BRAFIELDA. E. (1964) The oxygen content of interstitial water in sandy shores. J. Anim. Ecol. 33, 97-116. BRODY S. (1945) Bioenergctics and Growth, p. 355. Reinhold, New York. BULLOCK T. H. (1955) Compensation for temperature in the metabolism and activity of poikilotherms. Biol. Rev. 30, 311-342. BURKY A. J. (1971) Biomass turnover, respiration and interpopulation variation in the stream limpet Ferressea rivularis (Say). Ecol. Monogr. 41, 235-251. DAVIESP. S. (1966) Physiological ecology of Patella-I. The effect of body size and temperature on metabolic rate. J. mur. Biol. Ass. U.K. 46, 647-658. DAVIES P. S. (1967) Physiological ecology of Pan&r-II. Effect of environmental acclimation on the metabolic rate. y. mar. Biol. Ass. U.K. 47, 61-74. DAVIS P. S. & TRIBE M. A. (1969) Temperature dependence of metabolic rate in animals. Nature, Lntd. 224, 723-724. DAVIESP. S. & WALKEY M. (1966) The effect of body size and temperature upon oxygen consumption of the cestode Schistocephalus solidus (Muller). Camp. Biochem. Physiol. 18,415-426. DEHNEL P. A. (1960) Effect of temperature and salinity on the oxygen consumption of two intertidal crabs. Biol. Bull. mar. biol. Lab., Woods Hole 126, 354-372. DEHNEL P. A. & MCCAUGHRAN D. A. (1964) GiII tissue respiration in two species of estuarine crabs. Camp. Biochem. Physiol. 13, 233-260. GREEN R. H. & HOBSONK. D. (1970) Spatial structure in a temperate intertidal community, with special emphasis on Gemma gemma (Pelecypoda: Mollusca). Ecology 51, 999-1011. HALCROWK. & Bon, C. M. (1967) The oxygen consumption and swimming activity of the amphipod Gammarus oceanicus at different temperatures. Comp. Biochem. Physiol. 23, 233-242. HANKSJ. E. (1953) A comparative study of the feeding habits of the boring snails, Polinices heros (Say) and Polinices duplicata (Say) as related to water temperature and salinity. Masters Thesis, University of New Hampshire. HEMMINC%ENA. M. (1960) Energy metabolism as related to body size and respiratory surfaces, and its evolution. Reports Steno Memorial Hospital & Nordiak Insulin Laboratorium IX, Pt. II. HOCHACHKAP. W. & S~MSRO G. N. (1968) The adaptation of enzymes to temperature. Cow@. Biochem. Physiol. 27, 659-668. 39

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; oxygen consumption ; respiration ; temperature ; size ;