effects of aerial exposure on oxygen consumption by the new zealand mussel perna canaliculus...

LJournal of Experimental Marine Biology and Ecology,230 (1998) 15–29

Effects of aerial exposure on oxygen consumption by theNew Zealand mussel Perna canaliculus (Gmelin, 1791) from

an intertidal habitat

*Islay D. Marsden , Mark A. WeatherheadZoology Department, University of Canterbury, Private Bag 4800, Christchurch, New Zealand

Received 29 March 1997; received in revised form 5 March 1998; accepted 26 March 1998

Abstract

Aquatic and aerial oxygen uptake were measured for Perna canaliculus (Gmelin) (length 20–60mm) collected from mid-tide and low tide levels of a rocky shore during summer and winter.Oxygen uptake increased with tissue dry weight in aquatic and to a lesser extent aerial conditionsat most temperatures investigated, 10, 15 and 208C in summer and 5, 10 and 158C in winter.Aerial exposure reduced oxygen uptake up to 87% of the aquatic value with greater reduction athigher exposure temperatures. Oxygen uptake was similar in mussels from both shore levels andthere was no pronounced increase in the aquatic oxygen consumption of mid-shore individuals.There was little evidence of seasonal adjustment in the aquatic oxygen uptake rate–temperature(R–T ) curve for mussels from either mid- or low-shore levels; generally oxygen uptake increasedat higher exposure temperatures. In contrast, oxygen uptake of P. canaliculus in air was generallyreduced at higher exposure temperatures, and there was a small seasonal acclimatory response.Calculations of the daily oxygen requirements of mussels from the two shore levels suggest energysavings of 35% for mid-shore mussels during summer due to reduced oxygen demand in aerialconditions at higher temperatures. 1998 Elsevier Science B.V. All rights reserved.

Keywords: Oxygen uptake; Aerial respiration; Perna canaliculus; Mussel ecophysiology

1. Introduction

While mussels are often regarded as typically sublittoral animals, many extend theirdistributions into mid or higher levels of the intertidal zone (Bayne et al., 1976a). Thosemussels occupying higher tidal levels are subjected to increased periods of aerial

*Corresponding author. Present address: NIWA, P.O. Box 8602, Christchurch, New Zealand.

0022-0981/98/$ – see front matter 1998 Elsevier Science B.V. All rights reserved.PI I : S0022-0981( 98 )00067-7

16 I.D. Marsden, M.A. Weatherhead / J. Exp. Mar. Biol. Ecol. 230 (1998) 15 –29

exposure, extremes of temperature and desiccation stress and a reduced feeding period(Griffiths, 1981a; Griffiths and Buffenstein, 1981; Widdows and Shick, 1985). Numer-ous studies have investigated the respiratory physiology of bivalves (Thompson andBayne, 1972; Bayne et al., 1976a,b; de Vooys, 1987) and most agree that temperature isamongst the most important factors affecting oxygen consumption of mussels duringboth aerial exposure and tidal submersion. It has also been shown that some, but not allmussel species are able to show modification of their oxygen uptake rate–temperaturecurves to compensate for seasonal temperature variation (Bayne et al., 1976c; Thomp-son, 1984; Vial et al., 1992).

Mussels may also adjust growth rates or show morphological differences associatedwith different environmental conditions. For example M. edulis and P. canaliculus fromhigher tidal levels possess thicker shells and larger adductor muscles (Lewis and Seed,1969; Hickman, 1979). Intertidal mussels and cockles may use biochemical or otherphysiological mechanisms to survive and assist recovery from hypoxia resulting fromexposure at low tide (de Zwaan and Wijsman, 1976; Shick et al., 1986; Zange et al.,1989). Finally, behavioural mechanisms such as shell gaping may also enhance survivalat higher tidal levels, where small shell movements can assist both the maintenance ofaerobic metabolism (Kennedy, 1976; Widdows et al., 1979a; Guderley et al., 1994) andthe removal of anaerobic waste products (Demers and Guderley, 1994).

One strategy commonly used by high shore intertidal bivalves when exposed to aerialconditions is a reduction in oxygen consumption (Newell, 1979). This effectivelyreduces total energy expenditure due to respiration (Clarke and Griffiths, 1990,Davenport and Chown, 1995). Different species of mussels vary in their ability to reducemetabolism, they also differ within a single species collected from different geographicalareas and between subtidal and intertidal habitats (Widdows and Shick, 1985). However,for most Perna spp. there is little comparative information.

The present study was designed to investigate the effects of temperature and seasonon aerial and aquatic oxygen consumption of the New Zealand greenshell mussel Pernacanaliculus (Gmelin) collected from low and mid-shore levels on the same rocky shore.This mussel extends to depths of 55 m (Powell, 1979) and is commercially grown usinglongline suspension techniques. There are some previous data on the aquatic respirationof subtidally cultured greenshell mussels (Waite, 1989; Marsden and Shumway, 1992),but no such data for intertidal mussels or values for aerial oxygen uptake. Kennedy(1976) suggested that the upward limit of P. canaliculus on New Zealand shores is dueto the inability of small mussels to survive aerial conditions. In our study we tested theability of small to medium size mussels to maintain aquatic rates of oxygen uptakefollowing aerial exposure.

2. Materials and methods

2.1. Collection and maintenance

Specimens of Perna canaliculus ranging from 20 to 60 mm shell length werecollected by hand from a gently sloping rocky platform at Taylors Mistake, Canterbury,

I.D. Marsden, M.A. Weatherhead / J. Exp. Mar. Biol. Ecol. 230 (1998) 15 –29 17

New Zealand during summer (December–February 1992) and winter (May–July 1992).Descriptions of this site and its physical characteristics are found in Knox (1953) anddetails of the mussel distributions given in Kennedy (1976). Mussels were collectedduring spring tides from the low tide level where the exposure time was between 1 and 3h per tidal cycle and mid-tide level approximately 1 m above the level of low watersprings, with exposure times of 4–6 h. The average seawater temperatures range is15–198C in summer and 8–118C in winter, with air temperatures of 10–238C in summerand 3–138C in winter. Groups of mussels were transported back to the laboratory within30 min of collection, cleaned of epibionts and maintained in a recirculating seawatersystem, salinity 34 ppt, at temperatures close to 108C in winter and 158C in summer.Each mussel was individually marked using a bee dot and individuals were allowed torecover for at least 24 h before experimentation.

2.2. Aquatic oxygen uptake

Measurements were made on a size range of individual mussels at temperatures of 10,15 and 208C in summer and 5, 10 and 158C in winter using closed box respirometrytechniques. Five mussels and a control without a mussel were recorded each time inrespirometers (volume approx 250 ml) containing pasteurised seawater within a waterbath. Mussels were allowed to acclimate for 24 h, after which the water was changedand vessels sealed using silicon rubber bungs. Vessels were allowed to equilibrate for 15min prior to the first reading. Oxygen levels were determined from 1-ml samples takenfrom the chamber and passed through a 70-ml microcell (Strathkelvin InstrumentsMC100 Microcell) connected to a Strathkelvin 1302 oxygen probe and Model 781oxygen meter. Recordings were made over a period of 3 h at appropriate time intervalsto obtain a representative rate. External P was not allowed to fall below 80%O2

saturation. At each temperature, measurements were made on 5–19 individuals.Readings were corrected to standard temperature and pressure and represented as

21microlitres O h . At the end of each experiment the mussel tissue was removed from2

the shell and weight recorded after drying at 608C for 3 days. This temperatureminimises lipid weight loss during the drying process.

2.3. Aerial oxygen uptake

Measurements were made on a size range of mussels using a Gilson Differentialrespirometer. Preliminary experiments have shown that it is not necessary to shake therespirometers when measuring aerial oxygen uptake. The temperatures were the same asthose described for the aquatic respiration for each season. Individuals were held inrespirometer flasks (approximate volume 150 ml) with a central well containing 0.1 mlKOH to absorb CO . Humidity levels within the chamber were above 75% RH with2

high levels being maintained by 1 ml of pasteurised seawater at the bottom of eachvessel. Two controls without mussels were used in each experiment to control forpotential changes in barometric pressure. Mussels were allowed to adapt to the exposuretemperature for 30 min before the first readings were taken. Between 7 and 30individuals were recorded at each temperature. Because of relatively low rates of oxygen


uptake, readings were taken at 30 min intervals for periods of 90–120 min. The rateswere corrected to STP and the dry weights obtained as described in Section 2.2.

3. Results

3.1. Effects of body size

b~Oxygen consumption values for P. canaliculus were fitted to the equation V 5 axO221~where V 5oxygen consumption in ml h ; x5tissue dry weight in grams; a5interceptO2

and b5weight exponent. Regression equations and correlation coefficients for linesrelating body dry weight to the aquatic and aerial oxygen consumption are shown inTable 1. These show a significant weight relationship in all aquatic conditions except forthose at 58C during winter and 108C in summer for mid-tide mussels. At these exposuretemperatures, oxygen uptake was generally suppressed in larger mussels. The weightrelationships for aerial respiration were less well defined and the weight exponents weremore variable. For mussels collected from mid-tide levels, a significant weightrelationship for aerial respiration was found only at the storage temperatures of 108C inwinter and 158C in summer. The mean weight exponents for aquatic and aerial oxygenuptake were 0.73 and 1.16 respectively.

Table 1aRegression equations relating oxygen consumption in air and water of Perna canaliculus to dry body weight

T Low tide Mid-tide

(8C) a b r SL% a b r SL%

WaterS 10 0.163 0.83 0.98 1 0.070 0.34 0.54 NSS 15 0.239 0.69 0.86 1 0.208 0.65 0.71 1S 20 0.300 0.75 0.96 1 0.362 0.87 0.99 1

W 5 0.023 0.10 0.14 NS 0.034 0.07 0.16 NSW 10 0.129 0.66 0.87 5 0.232 0.91 0.94 1W 15 0.179 0.57 0.81 1 0.263 0.74 0.90 1

AirS 10 0.043 0.72 0.78 5 0.069 0.72 0.31 NSS 15 0.125 1.30 0.77 5 0.071 1.43 0.69 5S 20 0.040 0.51 0.92 1 0.057 1.49 0.53 NS

W 5 0.075 2.27 0.94 1 0.006 0.08 0.13 NSW 10 0.079 0.99 0.71 5 0.069 0.83 0.91 1W 15 0.081 1.13 0.62 1 0.036 0.19 0.19 NSa Mussels were collected during winter (W) and summer (S) from low-tide and mid-tide levels.

b 2 1Equations are in the form y5axb where y5ml O h and x is the dry tissue weight in grams.2

T5exposure temperature; r5correlation coefficient; SL5significance level; NS5not significant.


3.2. Effects of exposure temperature

Temperature had a significant effect on oxygen consumption in mussels collectedfrom both low- and mid-tide levels and comparisons of the regression lines are shown inTable 2 (analysis of covariance, Snedecor and Cochran (1976)). At higher temperaturesaquatic oxygen consumption increased, but the weight exponent b was similar for allsamples except those from the mid-tide in winter. For aerial oxygen uptake, temperaturehad a significant effect but uptake was consistently reduced at higher exposuretemperatures. In addition, the slope of the regression lines differed for mussels collectedduring winter. The combined effects of body size, exposure temperature and season onoxygen uptake are illustrated in Fig. 1 using values derived from the regression linesincluded in Table 1.

3.3. Effects of aerial exposure

Aerial exposure significantly reduced oxygen consumption in individuals from bothlow- and mid-shore levels. There was considerable heterogeneity of the variancesbetween aerial and aquatic samples that prevented direct comparison using the usualANCOVA techniques. Instead data from the 24 sets were compared in pairs usingDuncan’s test. A summary of these are included in Table 3. Aerial exposure significantlyreduced oxygen consumption in all but one of the samples. The ratio of aerial to aquaticrespiration, calculated from the regression lines are shown in Table 4. Oxygen uptakewas reduced by up to 87% compared with aquatic respiration, especially at highertemperatures. Mid-tide mussels appear able to maintain aerial rates of oxygen uptakesimilar to aquatic rates, at 108C during summer and low-tide mussels showed a similarresponse at 58C in winter. The overall reduction was similar in individuals collectedfrom the two shore levels and there was no consistent pattern with exposure temperature.

3.4. Effects of shore level and season

Aquatic oxygen uptake at each exposure temperature was similar for mussels

Table 2Analyses of covariance showing the effects of temperature on oxygen uptake of P. canaliculus

Comparison T F df SL F df SL(8C) (slope) (%) (elevation) (%)

Aquatic, summer mid-tide 10, 15, 20 2.46 2:19 NS 20.54 2:21 1Aquatic, summer low-tide 10, 15, 20 0.81 2:23 NS 33.43 2:25 1Aquatic, winter mid-tide 5, 10, 15 12.65 2:11 1 46.16 2:13 1Aquatic, winter low-tide 5, 10, 15 2.18 2:13 NS 269.8 2:15 1Aerial, summer mid-tide 10, 15, 20 0.50 2:18 NS 6.4 2:20 1Aerial, summer low-tide 10, 15, 20 3.27 2:15 NS 9.46 2:17 1Aerial, winter mid-tide 5, 10, 15 4.03 2:34 5 48.69 2:34 1Aerial, winter low-tide 5, 10, 15 4.65 2:40 5 25.91 2:42 1

T5temperature; df5degrees of freedom; SL5significance level; NS5not significant.

20I.D

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21Fig. 1. Aerial and aquatic oxygen uptake (ml O h ) for small (dry weight 0.25 g) and intermediate (dry weight 0.75 g) P. canaliculus from mid- and low-tide levels2

during summer and winter. Values were estimated from the regression lines included in Table 1 and compared in Tables 2 and 3: circles, small mussels; squares,intermediate mussels; closed symbols, aquatic respiration; open symbols, aerial respiration.

I.D.

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Table 321Pair-wise comparison of oxygen uptake (ml h ) for P. canaliculus using Duncan’s test

aConditions 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24

S M 10 w 1 j

S M 10 a 2 j

S M 15 w 3 X X j

S M 15 a 4 X j

S M 20 w 5 X X X j

S M 20 a 6 X X X X j

S L 10 w 7 X X X X j

S L 10 a 8 X X X X X j

S L 15 w 9 X X X X X X j

S L 15 a 10 X X X X X j

S L 20 w 11 X X X X X X X j

S L 20 a 12 X X X X X X X X j

W M 5 w 19 X X X X X X X j

W M 5 a 14 X X X X X X X X X X X X X j

W M 10 w 15 X X X X X X X X X X j

W M 10 a 16 X X X X X X X X X X j

W M 15 w 17 X X X X X X X X X X X X j

W M 15 a 18 X X X X X X X X X X j

W L 5 w 19 X X X X X X X X X X X j

W L 5 a 20 X X X X X X X X X X X X X X X X X X j

W L 10 w 21 X X X X X X X X X X X X X X X j

W L 1O a 22 X X X X X X X X X X X X j

W L 15 w 23 X X X X X X X X X X X X X X X X X j

W L 15 a 24 X X X X X X X X X X X X X X j

a W5winter, S5summer; Temperature (8C); M5mid-tide, L5low tide; a5air, w5water.

X5significant difference between groups at the 5% significance level.


Table 4Ratios of aerial:aquatic oxygen uptake of P. canaliculus collected from low and mid-tide levels during summerand winter calculated for a mussel 1 g dry wt

T (8C) Low-tide Mid-tide

Summer 10 0.26:1 0.99:115 0.52:1 0.34:120 0.13:1 0.16:1

Winter 5 3.26:1 0.24:110 0.61:1 0.30:115 0.45:1 0.14:1

21Fig. 2. Effect of season on aerial oxygen uptake (ml O h ) for P. canaliculus dry weight 0.5 g. The error bars2

are S.E. of the regression lines included in Table 1: symbols, summer values; open symbols, winter values.


Table 52 1Daily oxygen uptake requirement (ml O day ) for P. canaliculus from mid- and low-tide levels, calculated2

for two length groups, small (30 mm shell length) and intermediate (50 mm shell length) mussels

Mid-tide Low-tide Savings (%)

Winter Small 1.07 1.13 5.06Large 2.82 2.37 None

Summer Small 1.26 1.95 35.37Large 2.84 4.4 35.10

collected from both shore levels (Table 3). Fig. 1 illustrates oxygen uptake calculated formussels collected during summer and winter from mid- and low-tide levels. Comparisonof the seasonal sample from both shore levels suggest that P. canaliculus showed noseasonal modification in oxygen uptake in aquatic conditions. These curves aretemperature dependent within the normal environmental range both in summer andwinter, suggesting that P. canaliculus lacks respiratory adaptations that can compensatefor both daily and seasonal temperature change. For individuals from both shore levels,aquatic respiration was more temperature dependent than aerial respiration. Someseasonal adjustment may occur in the aerial rates of oxygen consumption, where atranslation of the R–T curve to the right in the summer was apparent for musselscollected from both tide levels (Fig. 2).

3.5. Total oxygen requirements

The daily oxygen consumption for P. canaliculus depends on body size, season andexposure period. As mussels from the two shore levels show similar dry weight and shelllength relationships (Weatherhead, 1993) we estimated the daily oxygen requirementsfor mussels of 30 and 50 mm shell length. These results, included in Table 5 werecalculated using the winter and summer air and seawater temperatures and combinationsof the aerial and aquatic oxygen consumption rates for each season. These predict thatmussels from the mid-tide level would not consistently have a lower oxygen demandthan those from the low shore. Energy expenditure of mussels from both size groupswould be similar during winter, when temperatures are low. In contrast with this result,during summer, small and intermediate length mussels from the mid-tide level show a35% reduction in their total oxygen demand.

4. Discussion

The distribution patterns of Perna canaliculus around New Zealand suggest thismussel is typically a lower littoral and sublittoral species that extends its distributionupshore only in selected areas within the middle of its geographical range (Morton andMiller, 1973). Investigation of the oxygen uptake of these intertidal mussels suggeststhat they display a limited range of strategies predicted for other invertebrates exposed to


aerial conditions (Gilmor, 1982). These are essentially capacity adaptations aimed atreducing energy expenditure and promoting survival at higher tidal levels.

Numerous studies have been carried out on the aquatic respiration of mussels(Widdows, 1973; Bayne et al., 1976c; Baby and Menon, 1986; Vismann, 1990) over awide range of experimental conditions. Although this makes comparison between studiesdifficult, in most laboratory studies, the rates are regarded as active or routine rates ofoxygen uptake (Newell, 1976). Values recorded here for P. canaliculus fall in the lower

21 21part of the range 0.17–1.76 ml O h g given by other authors (Bayne et al., 1976c;2

Vial et al., 1992) for the aquatic oxygen consumption of mussels recorded close to theirusual environmental temperature. In our experiments, mussels were starved and allowed24 h to adjust to the exposure temperature. If the oxygen consumption rates from our

21 21study reflect a standard or inactive rate, then values close to 0.2 ml O h g at habitat2

temperatures are similar to previous values for this species (Marsden and Shumway,1992) and compare well with a number of other mussel species, including theintensively studied M. edulis (Bayne et al., 1976a; Widdows and Shick, 1985; Vismann,1990). In contrast, they are low compared with Perumytilus purpuratus (Vial et al.,1992) and Perna indica (Baby and Menon, 1992).

Perna is regarded as a subtropical genus within which individuals can often attaincommercial size within a year (Vakily, 1989; Cheung, 1991a; Shafee, 1992) Annuallength increments range between 73 and 92.5 mm, for P. perna from Venezuela, P.viridis from Malaysia and subtidal P. canaliculus from New Zealand (Hickman, 1979;Parulekar et al., 1982). From previous work on energy requirements of invertebrates itmight be expected that molluscs with fast growth rates may also have an elevatedmetabolic rate. Low aquatic oxygen uptake rates recorded here for P. canaliculus mayappear inconsistent with active metabolism, short life span and rapid growth rate in thisgenus. However, two other factors may be important in explaining this apparentanomaly. The first considers maximum body size, where weight specific respiration isexpected to decrease with increasing body size (Newell, 1976). There are few values forPerna spp. that allow direct comparison, but our estimate for P. perna (calculated from

21 21Berry and Schleyer, 1983) is 0.42 ml g h at 208C. This value is similar to P.canaliculus and supports the general rule of reduced metabolic rate associated withlarger body size. The second factor likely to affect patterns of energy expenditure ofinvertebrates is food quality, quantity and availability. Branch and Newell (1978)predicted that limpet species living at a shore level with ample food resources wouldpossess a high metabolic rate and temperature sensitivity of the oxygen rate temperaturecurve. In contrast, those animals with an irregular or reduced food supply would showlow rates of metabolism and mechanisms for reducing energy expenditure. P.canaliculus from intertidal habitats appear to follow this latter pattern of metabolicadaptation.

When exposed to aerial conditions, some intertidal bivalves respire at a rate similar tothat in water (Widdows and Shick, 1985); however, apart from M. californianus (Bayneet al., 1976b) and Geukensia demissa (Kuenzler, 1961; Widdows et al., 1979a), this isnot a general feature of mussels. While most show a reduction in oxygen uptakefollowing aerial exposure, this may be less pronounced in those species found at high-and mid-tide levels than those that typically occur in subtidal habitats (Vial et al., 1992).


Some of the mytilids, including M. edulis, M. galloprovincialis (Widdows et al., 1979a)and Choromytilus meridionalis (Griffiths, 1981a) show a similar response to P.canaliculus, with reductions of up to 80% in their oxygen uptake following aerialexposure.

For many invertebrates, temperature change during aerial exposure might represent asignificant stress factor affecting oxygen consumption. Rates of oxygen uptake followingaerial exposure may be minimal representing the basal or standard rate as described byNewell (1976). By contrast with more active rates, the standard rates may be relativelytemperature independent over a wide temperature range. In our study, as in P.purpuratus (Vial et al., 1992), there was a significant effect of temperature on aerialoxygen uptake for low shore mussels. However, this was not a direct relationship withincreasing exposure temperature, and the highest rates were at the temperature mostsimilar to the seawater temperature for that season. However limited, the ability of P.canaliculus to use atmospheric oxygen during tidal emersion provides the opportunityfor maintaining basal metabolism, the chance to remove anaerobic waste productsproduced as a result of hypoxia, and allow for continued food digestion and assimilation.Research on M. edulis suggests that mussels from higher tidal levels, exposed toprolonged emersion acquire respiratory responses to adapt to hypoxic conditions andassist recovery patterns (Widdows and Shick, 1985; Shick et al., 1986; Demers andGuderley, 1994). P. canaliculus from higher tidal levels do not show increased abilityfor aerial respiration during air exposure, indeed our results suggest that mid-tidemussels may be considerably stressed compared with their lower shore counterparts.

Consistent with studies on C. meridionalis from South Africa (Griffiths, 1981a), bothaerial and aquatic oxygen uptake rates for P. canaliculus were size dependent, with asimilar weight dependence at a number of exposure temperatures. Average slope valuesfor aquatic respiration were similar to that recorded for other mussels (Bayne et al.,1976c; Sukhotin, 1992) and there was no difference in mussels from mid- and low-shorelevels. Variation in weight specific aquatic oxygen consumption with shore level hasbeen recorded for mussels including M. galloprovincialis (Dalla Via et al., 1987). Asnoted previously, the weight exponents for aerial respiration in P. canaliculus were morevariable than for aquatic respiration, and in mid-tide mussels, oxygen uptake wasindependent of body size. In this respect P. canaliculus shows similarities to M. edulis(Kuenzler, 1961; Coleman, 1973). This inability of mussels to increase aerial respirationwith increasing body size may reflect differences in conditions within the mantle cavity,where individuals may retain different quantities of fluid within the shell and gills, andother tissues become variously depressed. Individual P. canaliculus may also show sizerelated differences in shell opening patterns and desiccation rates that could affectoxygen uptake (Kennedy, 1976).

The effect of temperature on aquatic oxygen consumption in P. canaliculus followsthat of other mussels (Bayne et al., 1976c) where an increase in exposure temperatureresults in elevated oxygen consumption at higher temperatures. Q10 values of between1.3 and 2 at habitat temperatures between 10 and 208C are low but similar to those forgenera that include Perna, Mytilus and Modiolus (Widdows, 1973; Bayne et al., 1976a;Griffiths, 1981a). Temperature affected aquatic oxygen in New Zealand mussels frommid- and low-shore levels similarly, a feature also noted in Dalla Via et al. (1987).


However, for both C. meridonalis and M. galloprovincialis, mussels from mid-tidelevels showed elevated oxygen consumption, up to 45%, compared with their lowershore counterparts (Griffiths, 1981a; Dalla Via et al., 1987). No such dramatic increasein aquatic respiration was evident for P. canaliculus collected from mid-shore levels.

Griffiths (1981a) investigated the ability of the mussel, C. meridionalis, to modifyoxygen uptake in response to seasonal environmental change and concluded that subtidaland intertidal mussels do not show seasonal acclimatization. A similar pattern was foundfor P. canaliculus for aquatic respiration in our study. There was however, some supportfor such an adjustment, for aerial respiration, where a shift in the R–T curve resulted inhigher oxygen uptake at 108C in the winter than the summer. These seasonal patterns inaerial oxygen uptake of P. canaliculus help reduce overall energy consumption inmid-tide mussels during summer, when both sea and air temperatures are high. Musselsize did not affect the extent of metabolic savings, suggesting that small mussels are notbetter equipped to conserve energy through respiration than those of intermediate size.

Energy savings, a result of reduced oxygen demand during aerial exposure were sizedependent for the South African mussel, C. meridionalis (Griffiths, 1981a). Thepredicted annual respiratory costs for small mussels (20 mm shell length) were similarfor subtidal and intertidal groups of mussels, but there was an estimated 13% saving forintermediate (35 mm length) mussels, with even greater advantage predicted for largermussels. While our study confirms the general trends of energy savings in mussels fromhigher shore levels, it is clear that our estimates must be treated with caution. We did notinvestigate oxygen consumption during the recovery period, where in some bivalves,oxygen levels may be elevated for up to 2 h (Widdows and Shick, 1985). It is also notknown whether P. canaliculus uses the anaerobic metabolic pathways found in othermussels (de Vooys, 1987).

In studying the energetics of any bivalve, respiratory costs utilise a large proportion ofthe ingested energy (Widdows et al., 1979b; Sukhotin, 1992; van Haren and Kooijman,1993; Clausen and Riisgard, 1996). We measured standard rather than active rate ofmetabolism and preliminary research by Waite (1989) suggests a 1.5 times increase inoxygen consumption with a tenfold increase in food concentration. At even higher foodlevels, there may be further metabolic demands associated with particle selection, sortingor rejection as pseudofaeces (Bayne et al., 1989; Navarro et al., 1991). Differences infood levels and reduction in food availability due to tidal emersion have been suggestedas reasons why some intertidal mussels grow more slowly than subtidal individuals ofthe same species (Seed, 1969; Griffiths, 1981b; Shafee, 1992; Sukhotin and Kulakowski,1992). P. canaliculus from mid-tide levels have heavier shells and lower condition indexthan subtidal individuals (Weatherhead, 1993; Hickman and Illingworth, 1980). While itis likely that the shells of mid-tide individuals provide protection from desiccation andpredation pressure they may also require more energy for growth (Cheung, 1991b),muscle development, maintenance and functioning during opening and closing. It isclear that any future studies attempting to understand the energetics of P. canaliculusneed investigate these aspects further. Finally, as the respiratory responses recorded hereare for P. canaliculus collected from intertidal habitats, care should be used inextrapolating these results to subtidal habitats where different combinations of en-vironmental factor are likely to be in place.


Acknowledgements

We thank J. Hill and G. Robinson for technical assistance. Thanks also to A. Stewartand H. and L. Weatherhead for their support and help in completing the M.Sc. thesis.

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effects of aerial exposure on oxygen consumption by the new zealand mussel perna canaliculus...

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