effects of food concentration on clearance rate and energy budget of the arctic bivalve hiatella...

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Effects of food concentration on clearance rate and energy budget of the Arctic bivalve Hiatella arctica (L) at subzero temperature Mikael K. Sejr a, * , Jens K. Petersen a , K. Thomas Jensen b , Søren Rysgaard a a Department of Marine Ecology, National Environmental Research Institute. Frederiksborgvej 399 P.O. Box 358, 4000 Roskilde and Vejlsøvej 25 P.O. Box 314, 8600 Silkeborg, Denmark b Department of Marine Ecology, University of Aarhus. Finlandsgade 14, 8200 A ˚ rhus N, Denmark Received 13 November 2003; received in revised form 9 March 2004; accepted 14 May 2004 Abstract The influence of food concentration on clearance rate, respiration, assimilation, and excretion at 1.3 jC was studied on individuals of the bivalve Hiatella arctica (L.) from Young Sound, NE Greenland. Clearance rate, assimilation efficiency, respiration, and excretion rates were determined over a range of food concentrations using the microalga Rhodomonas baltica as food source. Physiological rates were generally low but responded significantly to increased food levels. Clearance rates and assimilation efficiency were reduced at increased food levels, whereas respiration and excretion increased. Assimilation efficiency was generally high, which may be an adaptation to the low food concentration during most of the year in NE Greenland. Low filtration rates limited ingestion rates and resulted in a low maximum assimilation of 3 J h 1 . Despite the low food intake, very low food concentrations were required for individual specimens to obtain a positive energy budget. Predicted growth based on rates of assimilation and respiration were compared to published estimates of annual growth in Young Sound. We estimate that 3 weeks of growth in the laboratory under optimal food conditions could match annual growth in situ. We interpret this as evidence that food limitation is the primary impediment to growth in this Arctic population. D 2004 Elsevier B.V. All rights reserved. Keywords: Metabolic rate; Hiatella arctica; Clearance rate 0022-0981/$ - see front matter D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2004.05.005 * Corresponding author. Tel.: +45-8920-1564; fax: +45-8920-1414. E-mail address: [email protected] (M.K. Sejr). www.elsevier.com/locate/jembe Journal of Experimental Marine Biology and Ecology 311 (2004) 171 – 183

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www.elsevier.com/locate/jembe

Journal of Experimental Marine Biology and Ecology

311 (2004) 171–183

Effects of food concentration on clearance rate and

energy budget of the Arctic bivalve Hiatella arctica

(L) at subzero temperature

Mikael K. Sejra,*, Jens K. Petersena, K. Thomas Jensenb,Søren Rysgaarda

aDepartment of Marine Ecology, National Environmental Research Institute. Frederiksborgvej 399 P.O. Box 358,

4000 Roskilde and Vejlsøvej 25 P.O. Box 314, 8600 Silkeborg, DenmarkbDepartment of Marine Ecology, University of Aarhus. Finlandsgade 14, 8200 Arhus N, Denmark

Received 13 November 2003; received in revised form 9 March 2004; accepted 14 May 2004

Abstract

The influence of food concentration on clearance rate, respiration, assimilation, and excretion at

� 1.3 jC was studied on individuals of the bivalve Hiatella arctica (L.) from Young Sound, NE

Greenland. Clearance rate, assimilation efficiency, respiration, and excretion rates were determined

over a range of food concentrations using the microalga Rhodomonas baltica as food source.

Physiological rates were generally low but responded significantly to increased food levels.

Clearance rates and assimilation efficiency were reduced at increased food levels, whereas

respiration and excretion increased. Assimilation efficiency was generally high, which may be an

adaptation to the low food concentration during most of the year in NE Greenland. Low filtration

rates limited ingestion rates and resulted in a low maximum assimilation of 3 J h� 1. Despite the low

food intake, very low food concentrations were required for individual specimens to obtain a positive

energy budget. Predicted growth based on rates of assimilation and respiration were compared to

published estimates of annual growth in Young Sound. We estimate that 3 weeks of growth in the

laboratory under optimal food conditions could match annual growth in situ. We interpret this as

evidence that food limitation is the primary impediment to growth in this Arctic population.

D 2004 Elsevier B.V. All rights reserved.

Keywords: Metabolic rate; Hiatella arctica; Clearance rate

0022-0981/$ - see front matter D 2004 Elsevier B.V. All rights reserved.

doi:10.1016/j.jembe.2004.05.005

* Corresponding author. Tel.: +45-8920-1564; fax: +45-8920-1414.

E-mail address: [email protected] (M.K. Sejr).

M.K. Sejr et al. / J. Exp. Mar. Biol. Ecol. 311 (2004) 171–183172

1. Introduction

In Polar regions, benthic invertebrates experience a unique combination of constant

low temperature ( <� 1 jC) and highly seasonal food supply (Clarke, 1998; Grebmeier

and Barry, 1991). The physical environment has pronounced influence on the population

dynamics and physiology of the populations present. Most notably, growth and P/B

ratios seem to be lower compared to species from warmer water, and longevity is usually

prolonged (Brey and Clarke, 1993). However, the relative influence of temperature and

food level varies between species. In general, studies from the Antarctic have shown that

low temperature limits metabolism. This causes the maximum energetic output to be

lower which can limit growth rates during periods of high food levels (Peck, 2002). In

some species, the thermally induced limits to activity is counteracted by increasing either

mitochondrial densities (Clarke, 1998)) or RNA/protein ratios (Fraser et al., 2002).

However, low metabolism can also work in favour of the organism, because it reduces

metabolic expenses, and hence the need for stored energy during low food levels in

winter (Brockington, 2001). The annual production is therefore affected by the

relationship between the length of the winter where no feeding occurs, the minimal

metabolic rate during low food levels, and the maximum metabolic rate during adequate

food level (Brockington, 2001). Because most Antarctic species exhibit pronounced

seasonality in both metabolism and growth related to changes in food supply (e.g.,

Brockington, 2001; Fraser et al., 2002; Brockington and Clarke, 2001), this has been

taken as evidence that food availability is the principal limitation to growth (Clarke,

1991).

Hiatella arctica is a widespread and abundant suspension-feeding bivalve in Arctic

coastal areas (Ockelmann, 1958). In Young Sound, NE Greenland it is one of the dominant

benthic species (Sejr et al., 2000) with ecological significance as a prey organism for

walruses (Born et al., 2003). Growth and production of H. arctica in Young Sound is

typical for a polar species. Production to biomass ratio is 0.095, annual growth is slow, and

maximum age is >120 years (Sejr et al., 2002a). In this study, we try to determine the

physiological basis for the slow annual growth observed by measuring clearance rate (CR),

respiration (R), excretion (E), and assimilation efficiency (AE) experimentally at varying

food levels but at a constant temperature of � 1.3 jC to simulate in situ conditions

(Rysgaard et al., 1998). Based on these measurements, we discuss the importance of food

and temperature as regulators of growth in the natural population of H. arctica in Young

Sound, NE Greenland.

2. Materials and methods

Specimens of H. arctica were collected in Young Sound, northeast Greenland

(74j18.58VN, 20j15.04VW) by divers during August 2000 and transported at � 1 to 0

jC to the National Environmental Research Institute, Denmark, within 2 days. The

clams were kept in filtered seawater with a salinity of approximately 31x, similar to

conditions in Greenland (Rysgaard et al., 1999). Temperature was controlled by

conducting experiments in a climate room set at � 1.3 jC. Water temperature was

M.K. Sejr et al. / J. Exp. Mar. Biol. Ecol. 311 (2004) 171–183 173

maintained at � 1.3F 0.1 jC throughout the experiments. Clams were acclimated to

laboratory conditions for 2 weeks before measurements were initiated. All shells were

cleaned of epibiota during the acclimation period. The flagellate microalga Rhodomonas

sp. was used as food source because of its use in similar experiments (e.g., Petersen

et al., 2003; Clausen and Riisgard, 1996). Cells of Rhodomonas sp. are almost spherical

with a diameter of 6 to 9 Am. The particle size for 100% retention efficiency in H.

arctica is about 3 Am (results not shown). The energy content of alga cells is 1.75 AJcell� 1 (Kiørboe et al., 1985), and the relationship between cell concentration (C, � 103

cells ml� 1) and chlorophyll a (Ag chl a l� 1) is chl a = 1.251�C (Clausen and Riisgard,

1996).

Measurements of clearance rate (CR), respiration (R), excretion (E), and assimilation

efficiency (AE) were performed as described below on a total of 51 clams ranging in size

from 0.046 to 0.785 g dry weight corresponding to a shell length of 1 to 5 cm. Dry weight

(dw) was determined by dissecting out the soft parts of individual clams and drying them

at 105 jC for 20 h.

Two 75-l tanks containing filtered (0.45 Am) seawater and the desired concentration

of algae were connected to a set of four Plexiglas chambers covered with gas-tight

floating lids. One clam was placed in each of three chambers, while the fourth

chamber served as a control. Two chamber volumes, 220 and 345 ml with a constant

water exchange rate of 10 to 20 ml min� 1, were used during each experiment. Water

in the chambers was thoroughly mixed using a 3-cm Teflon-coated magnetic stir bar

adjusted to 60 rpm. At each food level, clams were placed in chambers and left for a

minimum of 16 h. This allowed each individual time to acclimate to chambers and

food rations and ensured that enough faeces was produced for determination of

assimilation efficiency. By adjusting flow rates, we were able to ensure that the

oxygen concentration matched in situ conditions during the experiment (see details

later).

Two sets of experiments were conducted: (1) clearance rate (CR), assimilation

efficiency (AE), respiration (R), and excretion (E) were measured in specimens of different

sizes at a constant food level of 1854F 308 cells ml� 1 (meanF S.D.) in order to develop

relations between body size and physiological rates. The relationships were described by

allometric equations of the form Y= a X b, where Y is the physiological rate, X is the body

weight, and a and b are the fitted parameters. (2) Experiments were done to determine

effects of food level on the physiological rates. Rates were measured in clams of roughly

similar size (range: 0.46 to 0.67 g dw) at different alga concentrations (0–27,000 cells

ml� 1) and standardised to 0.5 g dw using the following formula (Navarro and Thompson,

1996):

Ys ¼ ðWs=WeÞbYe ð1Þ

where Ys is the physiological rate in an individual of standard weight, Ws is the standard

weight of individual, We is the observed weight of individual, Ye is the measured

physiological rate, and b is the weight exponent of the physiological rate function

determined from the regression equation.

M.K. Sejr et al. / J. Exp. Mar. Biol. Ecol. 311 (2004) 171–183174

2.1. Clearance rates

Clearance rate defined as clearance of 100% efficiently retained particles was measured

using the clearance method (Riisgard, 2001). When clams had acclimated to experimental

chambers and were open and filtering, the flow through each chamber was stopped and the

decrease in alga concentration was measured using a Coulter Multisizer II fitted with a

70-Am orifice tube. Four triplicate samples were collected from each chamber during a

1-h period. Clearance rate (CR) was determined from the exponential reduction of algal

cells as a function of time:

CR ¼ V=t � lnðC0=CtÞ ð2Þ

where V is the volume in the experimental chamber, t the time, and C0 and Ct the algal

cell concentration at times 0 and t, respectively. After collection of the four samples, the

flow was resumed until the initial alga concentration was restored. Each clam was left

for at least 1 h at the initial algal cell concentration before a new estimate of clearance

rate was obtained. Three estimates of clearance rate were obtained for each clam. The

food level of each clam was expressed as a mean value of C0.

2.2. Assimilation efficiency

Assimilation efficiency (AE) was estimated from collected faeces after measurements

of clearance rates had been completed. Faeces were collected with a pipette from

chambers and transferred to ashed (540 jC for 20 h), rinsed, and preweighed with 25-

mm Whatman GF/F filters. The filters were dried at 105 jC for 24 h to obtain total dry

weight, then ashed at 540 jC for 5 h, and reweighed to determine the organic content. The

ash-ratio method (Conover, 1966) was used to estimate assimilation efficiencies as given

by the formula:

AE ¼ ðf � eÞ � 100=ð1� eÞf ð3Þ

where AE is the assimilation efficiency, f is the organic fraction of food, and e is the

organic fraction of faeces.

2.3. Respiration

After collection of faeces, flow was kept constant for at least 1 h after the initial alga

concentration was restored. The flow was then shut off, and chambers were covered with

gas-tight floating lids. The inner diameter of the chambers exceeded the diameter of the

lids by f 2 mm. Tests showed that the O2 transport across lid and walls into the chambers

amounted to less than 3% of the lowest respiration rates measured. All respiration rates

were corrected for this and for respiration in the control chamber. Through initial

measurements, we determined the flow necessary to keep oxygen concentrations constant

and near saturation, and we showed that the oxygen concentration decreased linearly when

the flow was stopped. Thus, duplicate 5-ml samples were collected at the beginning and

end of the 3–4 h incubation period, and the O2 content was determined by Winkler

M.K. Sejr et al. / J. Exp. Mar. Biol. Ecol. 311 (2004) 171–183 175

titration (Strickland and Parsons, 1972). Oxygen saturation during the incubation period

generally decreased to about 85%, but a few individuals lowered the concentration to

75%. Rates were calculated from the slope of micromole O2 per clam against time for

different body sizes and alga concentrations. Rates are given as milligram O2 per hour and

were converted to joules per hour by using 14.0 J mg O2� 1 according to Tedengren et al.

(1990).

2.4. Excretion

Ammonium excretion rates (E) were determined by collecting samples of 3 ml each at

1-h intervals during the respiration experiment. Samples were passed through a 0.45-Amfilter and frozen until analysis. Analyses of ammonium contents were conducted using the

salicylate–hypochlorit method (Bower and Holm-Hansen, 1980). Rates of ammonium

excretion are given as microgram NH4–N per hour and were transformed to joule by

using the conversion factor 1 Ag NH4 = 0.025 J (Elliot and Davison, 1975). Clams for

respiration and excretion measurements at 0 cells ml� 1 were starved for 16 days prior to

experiments.

3. Results

Clearance, respiration, and excretion rates (CR, R, and E, respectively) of H. arctica

were all correlated with body size (Table 1). No significant relationship was observed

between assimilation efficiency (AE) and size. Assimilation was uniformly high in all

sizes of clams with an average of 82%F 1.3 (meanF S.E., n = 26). Physiological rates

were standardised to an individual with a body dw of 0.5 g using Eq. (1). The relationship

between CR and food level (Fig. 1) was best described by an exponentially decreasing

function (Table 2). Values ranged from 2 to 10 ml min� 1 with high variability in clearance

rates at low alga concentrations. Maximum CR was obtained at low food levels with cell

concentrations below 2000 cells ml� 1. For R and E, the relation between alga concen-

tration and physiological rate was fitted to an Ivlev model (Ivlev, 1961) modified by

including a positive y-axis intercept. Parameters of the fitted regression line are given in

Table 2. AE varied significantly with food level decreasing from around 90% at low food

concentrations to 32% at the highest food level. No production of pseudofaeces was

Table 1

Regressions of clearance rate (ml min� 1), assimilation efficiency (%), respiration rate (mg O2 h� 1), and excretion

rate (Ag NH4 h� 1) against dry weight

N R2 a b P

Clearance rate (CR) 26 0.80 14.84 0.58 < 0.01

Assimilation efficiency (AE) 26 0.06 81.03 � 0.01 NS

Respiration (R) 26 0.70 0.06 0.46 < 0.01

Excretion (E) 26 0.74 5.32 0.54 < 0.01

Regression equations are of the form Y= a DWb, where Y, physiological rate; DW, body dry weight; NS, not

significant (Hiatella arctica).

Fig. 1. Clearance rate (ml min� 1), assimilation efficiency (%), respiration rate (mg O2 h� 1), and excretion rate

(Ag NH4 h� 1) as a function of food level (cell ml� 1) standardised to a 0.5-g dry weight H. arctica individual.

Regression coefficients are given in Table 2.

M.K. Sejr et al. / J. Exp. Mar. Biol. Ecol. 311 (2004) 171–183176

observed during the experiments. The relationship between AE and food level was best

described by an exponential equation (Table 2).

4. Discussion

In this study, responses in physiological rates of H. arctica to body size or changes in

food supply are found to be similar to those observed at higher temperatures, except that

rates are lower (Clausen and Riisgard, 1996; Yukihira et al., 1998a; Navarro and Winter,

Table 2

Relationships between clearance rate (ml min� 1), assimilation efficiency (%), respiration rate (mg O2 h� 1) and

excretion rate (Ag NH4 h� 1), and food level (cells ml� 1) for a standard individual of 0.5 g dry weight (Hiatella

arctica)

N R2 Fitted model P

Clearance rate (CR) 29 0.74 CR= 8.41e� 0.0001�food conc. < 0.0001

Assimilation efficiency (AE) 29 0.86 AE= 0.91e� 0.00005�food conc. < 0.0001

Respiration (R) 35 0.91 R= 0.02 + 0.03(1–e� 0.00048�food conc.) < 0.0001

Excretion (E) 35 0.70 E= 1.79 + 4.71(1–e� 0.000066�food conc.) < 0.0001

M.K. Sejr et al. / J. Exp. Mar. Biol. Ecol. 311 (2004) 171–183 177

1982). The reduced clearance rate causes assimilation to decrease accordingly. Hence,

the maximum assimilated energy of a 0.5-g (dw) H. arctica individual was close to 3 J

h� 1, which is 12–25% of the maximum assimilated energy of other bivalves of the

same size but at higher temperatures (Yukihira et al., 1998a; Navarro and Winter, 1982).

However, the low respiration and excretion rates result in decreased energy require-

ments, and low food concentrations are sufficient to cover the expenses related to

maintenance metabolism, estimated as the mean respiration rate in starved animals.

Using a clearance rate of 10 ml min� 1 and an assimilation efficiency of 90%, we can

calculate that a food concentration of 268 cells ml� 1 (equivalent to 0.34 Ag chl a l� 1) is

required to cover the costs associated with maintenance. Using the same algae as food

source in a similar experiment Clausen and Riisgard (1996) found that at 15 jC, a 0.1-g

(dw) individual of the species Mytilus edulis needed 810 cells ml� 1. Thus, despite lower

feeding rates, H. arctica is able to maintain a positive energy budget even at low food

concentrations.

At high food concentrations, a decrease in clearance rate (CR) and assimilation

efficiency (AE) was observed. This is frequently observed in bivalves as a response to

satiation of the filtering and digestive system (Riisgard and Larsen, 2000). A decrease in

CR is often accomplished by reducing the valve opening (Dolmer, 2000; Jørgensen, 1990;

Riisgard, 2001), but in this study, low CR was observed in individuals with fully open

valves and extended siphon. Instead, a narrowing of the inhalent and exhalent siphon

openings was observed at high food levels. The decrease in CR and AE causes a drop in

the assimilated energy (Fig. 2). Although reported for other species (Yukihira et al.,

1998b), this is somewhat surprising. At high cell concentration, even small changes in CR

Fig. 2. Assimilated energy (J h� 1) as a function of food level in 0.5 g dry weight H. arctica individuals. Food

levels are given in cells ml� 1 (bottom axis) and Ag chl a l� 1 (top axis).

M.K. Sejr et al. / J. Exp. Mar. Biol. Ecol. 311 (2004) 171–183178

and AE will greatly affect the amount of assimilated energy and the observed drop could

be a result of slight inaccuracies in the determination of CR and AE.

The increase in oxygen uptake rate following feeding has been termed specific dynamic

action (SDA). From data on clearance rate and assimilation efficiency, the amount of

assimilated energy can be calculated and plotted against respiration rate (Fig. 3). The SDA

coefficient found as the slope of the fitted linear regression of respiration versus

assimilated energy (Fig. 3) is 0.15F 0.014 (S.E.). This corresponds to values generally

reported in the literature (Kiørboe, 1988). From the SDA coefficient and the theoretical

relationship between assimilation and growth (Kiørboe 1989, see below), the cost of

growth (dr/dg) can be estimated to 0.18 J per J biomass produced. This is a relatively low

cost of growth, meaning that production in H. arctica is efficient. In a study on the oyster

Saccostrea commercialis (Bayne, 2000), the cost of growth in control oysters was 0.81 J

J� 1. However, in fourth-generation oysters selected for high growth rates, the cost of

growth was reduced to 0.34 J J� 1. This demonstrates high plasticity of physiological rates

and the ability of bivalves to adapt to different selection regimes. Because polar benthos is

generally believed to be food limited (Clarke, 1998), it seems reasonable that selection has

favoured individuals with high growth efficiencies.

In H. arctica, respiration rates of fed individuals increase by a factor of 2.5 compared to

starved individuals (Fig. 3). This is similar to the increase of a factor of 1.6 to 2.5 found in

Antarctic ectotherms compiled by Peck (1998). Assuming that the range of factorial

increase in respiration is similar in Antarctic and Arctic species, this indicates that

metabolism in starved individuals can be used to approximate winter metabolism. A large

component of the SDA response is a result of elevated rates of protein synthesis (Peck,

1998). Although the fractional increase in respiration rate following feeding is comparable

Fig. 3. Respiration rate (J h� 1) as a function of assimilated energy (J h� 1) in a 0.5-g dry weight H. arctica

individual. Linear regression: respiration = 0.31 + 0.15� assimilation. N= 35, F = 112; P < 0.0001.

M.K. Sejr et al. / J. Exp. Mar. Biol. Ecol. 311 (2004) 171–183 179

in Arctic and boreal species, the absolute energy output is lower for individuals living at

low temperature (Peck, 2002). The lower energy output combined with lower assimilation

rate reduces the maximum rate of protein synthesis in cold-water ectotherms.

The cost of growth calculated from the SDA above can be used to estimate growth rates

from the respiration and assimilation rates found in this study. According to Kiørboe

(1989) growth ( g) can be defined as the difference between assimilation (a), and

metabolism (r):

g ¼ a� r

Assuming linear relationships between g, a, and r, differentiation of this equation with

respect to assimilation yields:

dr=daþ dg=da ¼ 1

and

ðdr=daÞ=ðdg=daÞ ¼ dr=dg

where dr/da is the slope of the linear relationship between respiration (r) and assimilation

(a) or the SDA coefficient, dg/da is the slope of the linear relationship between growth ( g)

and assimilation, and dr/dg is the slope of the relationship between respiration and growth,

which is also an estimate of the cost of growth. From Fig. 3, we get an estimate of dr/da,which can be used to calculate dg/da. Because the intercept of the regression of growth on

assimilation is the standard metabolism estimated in starved individuals, we can use this

relation to predict growth from the amount of assimilated energy measured. The maximum

assimilation rate is 1.2 J h� 1. Using the above relationship, it corresponds to a deposition

of biomass equivalent to 0.9 J h� 1. Mean annual growth under natural conditions has been

studied in H. arctica in Young Sound, NE Greenland (Sejr et al., 2002a). On the basis of

annual growth lines in the shell (Sejr et al., 2002b), individual age was estimated and

plotted against shell length to estimate average growth in the population. Growth was

slow, with a maximum age of 126 years. The mean individual annual growth estimated

from the fitted von Bertalanffy growth function was 24 mg dw year� 1 (Sejr et al., 2002a).

The energetic content in soft tissue from H. arctica has been measured at 492 J 24 mg� 1

(Born et al., 2003). The deposition rate of 0.9 J h� 1 calculated above implies that under

optimal food conditions, individuals in the laboratory would be able to achieve the annual

growth estimated in Young Sound in only 23 days.

In our experimental setup, we have simulated conditions in Young Sound, i.e., highly

varying food concentrations and constant low temperatures. Low temperature clearly

limits clearance rates of H. arctica in Young Sound (Petersen et al., 2003). Consequently,

less energy is assimilated and available for growth. Furthermore, low temperature also

slows down metabolism and limits maximum rates of biosynthesis (Clarke, 1998; Peck,

1998). Hence, the overall growth potential of a polar bivalve will be lower compared to

species inhabiting a similar ecological niche at a higher temperature. The calculated rate of

biomass deposition in this study does not estimate growth in nature. It is an estimate of the

maximum growth potential of this species at low temperature and optimal food conditions.

It is predicted from measured rates of respiration and assimilation assuming linear

relationships between respiration, assimilation, and growth linearity. Although this indirect

M.K. Sejr et al. / J. Exp. Mar. Biol. Ecol. 311 (2004) 171–183180

method is less precise than direct measurements of growth, we believe that the short period

(23 days) required for specimens in the laboratory to match the annual growth rate in

Young Sound, NE Greenland demonstrates that the growth potential is not fully exploited

in the natural population. Several factors might have caused us to overestimate the growth

rate in the laboratory: (1) animals used in the study were all collected in August. Because

spawning is usually in early Arctic summer (June–July), the mass of gonads were at a

minimum, reducing the basic metabolic expenses. (2) Using a monoculture of algae could

provide a food source of better quality than in nature causing assimilation efficiency to be

overestimated. However, mean annual assimilation efficiency of subarctic Modiolus

modiolus feeding on natural seston was found to be 77% (Navarro and Thompson,

1996) compared to our mean of 82%. Using an assimilation efficiency of 70% instead of

82%, increases the time required to match annual growth to 43 days. (3) A relative low

cost of growth was estimated from the relationship between respiration and assimilation.

Although it is comparable to estimates measured by more direct methods, it could cause

the period of 23 days to be underestimated. Applying a cost of growth of 0.34 as found by

Bayne (2000) alters the estimate to 39 days. We believe that our results show that H.

arctica is able to grow much faster at low temperatures than observed in Young Sound

when provided with food in the laboratory, and that despite the indirect approach used, the

conclusion is robust even when conservative values for assimilation efficiency and cost of

growth is applied.

The discrepancy between potential and realised growth in this population is most likely

a result of long periods during winter when food supply is below that which is required for

a positive energy budget. It is thus possible to separate the rate-limiting effect of low

temperature from the effect of seasonal resource limitations on the annual growth rate. Our

results suggest that despite the low rates of assimilation and growth caused by temperature,

low food availability is a major regulator of growth in this population. Young Sound is ice-

covered 9 months a year with a phytoplankton bloom lasting 3–6 weeks (Rysgaard et al.,

1999). Data from sediment traps show sedimentation of chl a from July to October in

Young Sound (Rysgaard et al., in press). However ice algae production takes place during

June (Nielsen et al., accepted for publication) Because only 0.34 Ag chl a l� 1 is required to

cover metabolic expenses in starved animal, we suggest that individuals of H. arctica

probably have a positive energy budget from June to October when ice forms again.

Assuming that no feeding takes place during the rest of the year and using metabolism in

starved individuals as an estimate of winter metabolism, this would require an individual

of 0.5 g to reduce its body energy content by 14% to cover expenses during the nonfeeding

period. This is comparable to the about 10% reduction in body energy content observed in

the Antarctic bivalve Laternula elleptica during winter (Brockington, 2001). Here, it was

also demonstrated that L. elliptica cease feeding during 4 months in the winter (Brock-

ington, 2001). The importance of food supply on the seasonal energetics of polar benthos

was also demonstrated for the sea urchin Sterechinus neumayeri (Brockington and Clarke,

2001). Here, it was estimated that temperature only accounted for 15–20% of the summer

increase in metabolism, whereas increased physiological activity associated with feeding,

growth, and spawning accounted for the remaining 80–85%. Different annual growth rate

of S. neumayeri at four sites McMurdo Sound was also related to differences in food

supply between the sites (Brey et al., 1995).

M.K. Sejr et al. / J. Exp. Mar. Biol. Ecol. 311 (2004) 171–183 181

The apparent resource limitation of the growth and production of H. arctica in Young

Sound is of interest because of the reduced ice cover in the Arctic (Serreze et al., 2000;

Johanneson et al., 2002). A reduction of ice cover and thus extension of the ice-free period

in Young Sound have been proposed to increase primary production in the area (Rysgaard

et al., 1999). This study suggests the if the amount of food available to the population of

H. arctica in Young Sound increases in the future, it will readily be converted into

increased annual growth and production.

Acknowledgements

This study was supported financially by the Danish Natural Science Research Council.

M.K. Sejr was supported by the Carlsberg Foundation (grant no ANS-1447/20). Egon R.

Frandsen and Kitte Gerlich are thanked for laboratory assistance. Finally, Anna Haxen is

acknowledged for linguistic corrections. [SS]

References

Bayne, B.L., 2000. Relations between variable rates of growth, metabolic cost and growth efficiencies in

individuals Sydney rock oysters (Saccostrea commercialis). J. Exp. Mar. Biol. Ecol. 251, 185–203.

Born, E.W., Rysgaard, S., Ehlme, G., Sejr, M.K., Acquarone, M., Levermann, N., 2003. Underwater observation

of foraging free-living walruses (Odobenus rosmarus) including estimates of their food consumption. Polar

Biol. 26, 348–357.

Bower, C., Holm-Hansen, T., 1980. A salicylate–hypochlorite method for determining ammonia in seawater.

Can. J. Fish. Aquat. Sci. 37, 794–798.

Brey, T., Clarke, A., 1993. Population dynamics of marine benthic invertebrates in Antarctic and subantarctic

environments: are there unique adaptations? Antarct. Sci. 5, 253–266.

Brey, T., Pearse, J., Basch, L., McClintock, J., Slattery, M., 1995. Growth and production of Sterechinus

neumayeri (Echinoidea: Echinodermata) in McMurdo Sound, Antarctica. Mar. Biol. 124, 279–292.

Brockington, S., 2001. The seasonal energetics of the Antarctic bivalve Laternula elleptica (King and Broderip)

at Rothera Point, Adelaide Island. Polar Biol. 24, 523–530.

Brockington, S., Clarke, A., 2001. The relative influence of temperature and food on the metabolism of a marine

invertebrate. J. Exp. Mar. Biol. Ecol. 258, 87–99.

Clarke, A., 1991. What is cold adaptation and how should we measure it? Am. Zool. 31, 81–92.

Clarke, A., 1998. Temperature and energetics: an introduction to cold ocean physiology. In: Portner, H.O., Playle,

R.C. (Eds.), Cold Ocean Physiology. Cambridge University Press, Cambridge, pp. 3–30.

Clausen, I., Riisgard, H.U., 1996. Growth, filtration and respiration in the mussel Mytilus edulis: no evidence for

physiological regulation on the filter-pump to nutritional needs. Mar. Ecol., Prog. Ser. 141, 37–45.

Conover, R., 1966. Assimilation of organic matter by zooplankton. Limnol. Oceanogr. 11, 338–354.

Dolmer, P., 2000. Feeding activity of mussels Mytilus edulis as related to near-bed currents and phytoplankton

biomass. J. Sea Res. 44, 221–231.

Elliot, J.M., Davison, W., 1975. Energy equivalents of oxygen consumption in animal energetics. Oecologia 19,

195–201.

Fraser, K.P.P., Clarke, A., Peck, L.S., 2002. Low-temperature protein metabolism: seasonal changes in protein

synthesis and RNA dynamics in the Antarctic limpet Nacella concinna Strebel 1908. J. Exp. Mar. Biol. Ecol.

205, 3077–3086.

Grebmeier, J.M., Barry, J.P., 1991. The influence of oceanographic processes on pelagic–benthic coupling in

Polar regions: a benthic perspective. J. Mar. Syst. 2, 495–518.

M.K. Sejr et al. / J. Exp. Mar. Biol. Ecol. 311 (2004) 171–183182

Ivlev, V.S., 1961. Experimental Ecology of the Feeding of Fishes. Yale Univ. Press, New Haven, USA.

Johannesson, O.M., Bengtsson, L., Miles, M.W., Kuzmina, S.I., Semenov, V.A., Alekseev, G.V., Nagurnyi, A.P.,

Zakharov, V.F., Bobylev, L., Pettersson, L., Hasselmann, K., Cattle, H.P., 2002. Arctic climate change—

observed and modelled temperature and sea ice variability. Technical Report no 218, p 22.

Jørgensen, C.B., 1990. Bivalve Filter Feeding: Hydrodynamics, Bioenergetics, Physiology and Ecology. Olsen &

Olsen, Fredensborg Denmark. 140 pp.

Kiørboe, T., 1988. Planktonfødekæden: Bioenergetiske og økologiske studier. Olsen & Olsen, Fredensborg.

80 pp.

Kiørboe, T., 1989. Growth in fish larvae: are they particularly efficient? Rapp. P.-v. Reu. Cons. Int. Explor.

Mer. 191, 383–389.

Kiørboe, T., Møhlenberg, F., Hamburger, K., 1985. Bioenergetics of the planktonic copepod Acartia tonsa:

relations between feeding, egg production and respiration, and composition of specific dynamic action.

Mar. Ecol., Prog. Ser. 26, 85–97.

Navarro, J.M., Thompson, R.J., 1996. Physiological energetics of the horse mussel Modiolus modiolus in a cold

ocean environment. Mar. Ecol., Prog. Ser. 138, 135–148.

Navarro, J.M., Winter, J.E., 1982. Ingestion rate, assimilation efficiency and energy balance in Mytilus chilensis

in relation to body size and different algal concentrations. Mar. Biol. 67, 255–266.

Nielsen, T.G., Ottosen, L.D., Hansen, B.W., accepted for publication. Structure and function of the pelagic

ecosystem in an ice covered Arctic fjord. In: Rysgaard, S., & Glud, R.N. (Eds.) Carbon cycling in Arctic

marine ecosystems: case study Young Sound. Meddr Greenland, Bioscience Special Issue.

Ockelmann, W.K., 1958. The zoology of east Greenland: marine Lamellibranchiata. Meddelelser om Grønland

122, 1–256.

Peck, L.S., 1998. Feeding, metabolism and metabolic scope in Antarctic marine ectotherms. In: Portner, H.O.,

Playle, R.C. (Eds.), Cold Ocean Physiology. Cambridge University Press, Cambrigde, pp. 365–390.

Peck, L.S., 2002. Ecophysiology of Antarctic ectoterms: limits to life. Polar Biol. 25, 31–40.

Petersen, J.K., Sejr, M.K., Larsen, J.E.N., 2003. Clearance rates in the Arctic bivalves Hiatella arctica and Mya

truncata. Polar Biol. 26, 334–341.

Riisgard, H.U., 2001. On measurement of filtration rates in bivalves—the stony road to reliable data: review and

interpretation. Mar. Ecol., Prog. Ser. 211, 275–291.

Riisgard, H.U., Larsen, P.S., 2000. Comparative ecophysiology of active zoobenthic filter feeding, essence of

current knowledge. J. Sea Res. 44, 169–193.

Rysgaard, S., Thamdrup, B., Risgaard-Petersen, N., Fossing, H., Berg, P., Christensen, P.B., Dalsgaard, T., 1998.

Seasonal carbon and nutrient mineralization in a high-Arctic coastal marine sediment, Young Sound, northeast

Greenland. Mar. Ecol., Prog. Ser. 175, 261–276.

Rysgaard, S., Nielsen, T.G., Hansen, B.W., 1999. Seasonal variation in nutrients, pelagic primary production and

grazing in a high-Arctic coastal marine ecosystem, Young Sound, northeast Greenland. Mar. Ecol., Prog. Ser.

179, 13–25.

Rysgaard, S., Frandsen, E., Sejr, M.K., Christensen, P.B., in press. The MarinBasic program-monitoring program

report 2002–2003. In: Caning, K., Rasch, M. (Eds.), ‘‘Zackenberg Ecological Research Operations, ZERO’’

8th Annual Report, 2003 Copenhagen. Danish Polar Center, Minestry of Science, Technology and Innovation

2004.

Sejr, M.K., Jensen, K.T., Rysgaard, S., 2000. Macrozoobenthic community structure in a high-Arctic East

Greenland fjord. Polar Biol. 23, 792–801.

Sejr, M.K., Sand, M.K., Jensen, K.T., Petersen, J.K., Christensen, P.B., Rysgaard, S., 2002a. Growth and

production of Hiatella arctica (Bivalvia) in a high-Arctic fjord (Young Sound, northeast Greenland). Mar.

Ecol. Prog. Ser. 244, 163–169.

Sejr, M.K., Jensen, K.T., Rysgaard, S., 2002b. Annual growth bands in the bivalve Hiatella arctica validated by a

mark-recapture study in NE Greenland. Polar Biol. 25, 794–796.

Serreze, M.C., Walsh, J.E., Chapin III, F.S., Osterkamp, T., Dyurgerov, M., Romanovsky, V., Oechel, W.C.,

Morison, J., Zhang, T., Barry, G., 2000. Observational evidence of recent change in the northern high-latitude

environment. Clim. Change 46, 59–207.

Strickland, J.D., Parsons, T.R., 1972. A Practical Handbook of Seawater Analysis, 2nd ed. Bull. Fish. Res. Can.,

vol. 167, p. 310.

Tedengren, M., Andre, C., Johannesson, K., Kautsky, N., 1990. Genotypic and phenotypic differences between

M.K. Sejr et al. / J. Exp. Mar. Biol. Ecol. 311 (2004) 171–183 183

baltic and North Sea populations of Mytilus edulis evaluated through reciprocal transplantations: III.

Physiology. Mar. Ecol. Prog. Ser. 59, 221–227.

Yukihira, H., Klumpp, D.W., Lucas, J.S., 1998a. Effects of body size on suspension feeding and energy budgets

of the pearl oysters Pinctada margaritifera and P. maixma. Mar. Ecol. Prog. Ser. 170, 119–130.

Yukihira, H., Klumpp, D.W., Lucas, J.S., 1998b. Comparative effects of microalgal species and food concen-

tration on suspension feeding and energy budgets of the pearl oysters Pinctada margaritifera and P. maxima

(Bivalvia: Pteriidae). Mar. Ecol. Prog. Ser. 171, 71–84.