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Physiological energetics of Japanese scallop Patinopecten yessoensis larvae
J. Exp. Mar. Biol. Ecol., 1988, Vol. 120, pp. 155-170 Elsevier
155
.JEM 01108
Physiological
energetics of Japanese scallop Patinopecten yessoensis larvae B.A. MacDonald
Rutgers ShellfTh Research Laboratory, Cook College, New Jersey Agricultural Experiment Station, Rutgers University, Port Norris, New Jersey. U.S.A. (Received
19 January
1988; revision
received
3 May 1988; accepted
7 May 1988)
Growth and ingestion rates were determined for Japanese scallop Patinopecten yessoensis larvae reared at temperatures between 10 and 18 “C and fed concentrations of Isochrysis aK galbana (clone T-ISO) cells between 5 and 30 cells . ply ’ to gain insight into energy balance. Veliger larvae were held in experimental chambers at densities of 0.5-100. ml ’ to assess the influence of crowding on growth, respiratory and feeding rates. Long-term growth studies lasting 28 days indicated that growth was most rapid at highest food concentrations of 30 cells . pl_ ’ despite indications from short-term feeding studies that ingestion was at a maximum and independent ofconcentration between 15 and 30 cells. ~1~ ‘. Growth and ingestion are both reduced as the density of larvae increases. Feeding rates (6 h) remained fairly constant between densities of l-5 larvae ml- ’ if food availability was increased proportionately. However, growth experiments lasting 28 days revealed extremely low survivorship if larvae are reared at densities of > 2 ml _ ‘. Respiratory rates were higher than previously reported for bivalve larvae and reaching values of 13 nl . h- ’ or 13-29 ml ~35% at larval densities between 5 and 0, g ’ [AFDW] h - ‘. Oxygen consumption was reduced 25 . ml ’ which are typical densities used when measuring metabolic rates of veliger larvae. Assimilation efficiencies between = 55 and 80% were comparable to published values for mussel and oyster larvae but higher respiratory demand and comparatively slow growth rates for this species were reflected in lower growth effkiencies than those previously reported for bivalve larvae. Japanese scallop larvae apparently require a minimum food concentration of 7-15 cells. ~1~ ’ (depending on size) to gain sufficient energy to support respiration and growth. Despite morphological similarities between species of bivalve larvae they may differ in their rates of energy acquisition and utilization. Abstract:
Key words: Energetics;
Feeding;
Growth;
Larva;
Respiration;
Scallop
INTRODUCTION
Planktotrophic marine larvae meet their nutritional requirements by filtering particulate material, primarily microalgae from the surrounding seawater, with the ciliated velum (Strathmann et al., 1972). Aspects of larval feeding behavior that vary in response to environmental conditions are of fundamental interest to physiological ecologists studying energy acquisition and utilization and are highly relevant to commercial hatcheries (Bayne, 1983). Energy intake has usually been determined by measuring
Contribution 734 from Marine Sciences Research Laboratory. Correspondence address: B.A. MacDonald, Marine Sciences Research of Newfoundland, St. John’s, Newfoundland AlC 5S7, Canada. 0022-0981/88/$03.50
0 1988 Elsevier
Science
Publishers
Laboratory,
B.V. (Biomedical
Division)
Memorial
University
156
B.A. MACDONALD
ingestion or filtration rates over short periods of time, and estimates of the energy requirements of feeding or swimming obtained by measuring rates of oxygen consumption using a variety of techniques (Sprung, 1984~). Long-term changes in growth and survival have been used as indicators of larval response to a range of environmental or hatchery conditions, because such changes represent the net result of all integrated physiological processes within the organism. Most of the information available on growth rates and feeding characteristics of molluscan larvae has been provided by studies on commercially important species grown in hatcheries at artificially high food levels. Feeding characteristics of larvae reared at ambient temperatures, a variety of food levels, including the low concentrations normally found in the natural environment, have recently been described for Mytilus edulis and Ostrea edulis (Sprung, 1984b; Crisp et al., 1985). The basic feeding response to increasing food concentrations exhibited by larvae in these studies was for ingestion to increase until reaching a plateau while filtration rate decreased steadily. Comparative studies such as these have revealed major differences in the energy requirements of oyster and mussel larvae, and suggest that the latter are capable of growing at food levels far lower than those required by the former (Crisp et al., 1985). A problem encountered when studying larvae is the need to enclose and concentrate them in order to detect measurable changes in feeding or metabolic rates over a short period (Sprung, 1984~). Larval densities in experimental containers have ranged from 1 to 100*mll (Walne 1966; Millar & Scott, 1967; Riisgkd et al., 1980, 1981; Fritz et al., 1984; Sprung, 1984a; Crisp et al., 1985; this study). Natural larval densities are obviously much lower, with maximum densities approaching 1200 * m - 3 or 0.0012. ml- ’ for Patinopecten yessoensis (Ventilla, 1982) and a mean of 0.002. ml ’ for Crassostrea virginica (Fritz et al., 1984). Reductions in feeding rate (Fritz et al., 1984) growth rate (Davis, 1953; Loosanoff & Davis, 1963; Malouf & Breese, 1977), and metabolic rate (Walne, 1966; Millar & Scott, 1967) have all been reported for bivalve larvae at greater densities. The degree of concentration could have a profound effect on larval behavior by greatly increasing the likelihood of one individual colliding with another, causing damage or an interruption in feeding activity, and by increasing the concentration of excretory products. Interpreting results obtained with dense cultures is rather difficult, and recent studies suggest that larval density is a factor worth considering. The Japanese scallop industry (P. yessoensis) represents a major portion of the world’s total scallop production and is currently supported by an extensive program to monitor natural larval abundances and spat collection (Mottet, 1979; Ventilla, 1982). Declines in several natural scallop fisheries, high market demand, and the success of the Japanese industry have prompted recent international interest in the potential benefits of culturing scallops. Insufficient or irregular natural recruitment for pectinids in several areas has resulted in studies on the feasibility of commercial-scale scallop hatcheries like those existing for oysters. In this study the rates of feeding, metabolism, and growth of larval P. yessoensis were
PHYSIOLO~ICALENERGETICS OF PATZ~~PECT~~YESSOE~SZS
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determined at food levels, temperatures, and larval densities appropriate to natural conditions and those encountered in hatcheries. The objectives of this study were to assess the energy requirements of larvae and to determine conditions for optimal growth. Comparisons will be made between conditions predicted to be optimal based on short-term feeding studies and those found to give the best results based on long-term growth studies.
MATERIALS AND METHODS SPAWNING AND REARING
Broodstock Japanese scallops F. yes.roe&s were held in quarantine and kept in spawning condition by holding them for at least 1 wk in 5-8 “C seawater and feeding them a mixture of Zsochrysis aff. galbana, Chaetoceros calcitrans, and Thalassiosira pseudonana. The following brief description of spawning and rearing conditions was taken from Thompson et al. (1985). Scallops were induced to spawn by removing them from seawater for R 1 h before being returned to water warmed to 12 or 15 “C or by an injection of 0.4 ml of 2 x 10W5M solution of serotonin into the adductor muscle. After the addition of sperm, fertilized eggs were gently washed and placed in seawater ( 14 ’ C) at a concen~ation of 4-l 1 eggs * ml - ’ and allowed to develop into trochophore (l-2 days) and veliger larvae (2-3 days). Developm~t~ stages and growth rates of P. yessoensis larvae in the natural environment have been provided by Maru (1972) and Ventilla (1982) (see Discussion). Larvae in this study achieved a mean shell length (D stage) of Q 120 pm ( RZ145 ng) 3 days after fertilization. These larvae metamorphosed x 30 days after fertilization when they reached a mean shell length of 250-260 pm and weighed between 900 and 1000 ng (Thompson et al., 1985; Whyte et al., 1987). Larvae were reared at a density of 1-2*ml- ’ in large fiberglass cylinders (0.35-6 m3) with a complete water exchange (15 “C) every 3-4 days. GROWTH
RATES
Larvae from the same large rearing tank (3 days old) were held at a density of 1 ind . ml - ’ in 4-l glass beakers cont~~g 3.5 1 of filtered seawater (1 pm) at ambient salinity (29 + 1“/,), and were fed exclusively on ZsochrySs af?‘.galbana (clone T-ISO) at concentrations of 5, 10, 15, 20, and 30 cells * ~1~ *. The influence of crowding was determined by maintaining food availability at 20 000 cells * larva- ’ while varying larval density (0.5, 1,2, 5, and 10 larvae *ml- ‘. Three replicate beakers were set up for each experimental treatment and placed in water baths at either 10, 14, or 18 “C. To keep food particles in suspension, each beaker was supplied with air from a line fitted with a glass pipette at the end to deliver small bubbles to the bottom of the chamber at rate of 1-2 bubbles * s - I. Particle counts were monitored frequently using a Coulter TAIr counter and adjusted if they varied by > 10% from original levels.
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Every 2-3 days larvae were concentrated on a 53-pm screen and resuspended in filtered water in a clean beaker. Once a week during routine water changes larvae were examined under a microscope equipped with a calibrated eyepiece graticule, and shell length ( it 5 pm) determined for 30 larvae selected at random in each replicate. Total dry weight and ash free dry weight were determined for various sizes of surplus groups of larvae after washing with distilled water and collecting them under vacuum on preashed and preweighed fiber glass filters (GF/C; 21 mm diameter). Filters were dried at 90 “C for several hours, weighed on an ultramicrobalance to & 1 pg, and then placed in a muffle furnace at 500 “C for 48 h before determining final ash weight. FEEDING
RATES
Larvae from one of three standardized size classes [mean shell length, small x 140 ,um (125-170 pm), medium z 200 pm (160-230 pm), large x 240 pm (200-270 pm)] were added (1 * ml- ‘) to 2-l glass beakers containing 1.8 1 of filtered seawater ( -=z1 pm). While the larvae used for growth studies were from the same batch those individuals used for short-term feeding and metabolic studies were from different batches that had received similar treatment. Three experimental and one control beaker (without larvae) were set up with aeration and placed in water baths at either 10, 14, or 18 “C at each of the following concentrations: 5, 10, 15,20, and 30 cells * pl- r. The use of control beakers made it possible to determine whether changes in particle counts were unrelated to larval feeding, such as cells dividing or settling, and whether the smallest larvae were feeding at all. After an initial adjustment period of z 2 h, 25 ml samples were removed from each beaker every 30-60 min and passed through a 53-pm screen to remove larvae. Isochrysis cells were counted five times for each sample using a Coulter TA,, counter fitted with a 50-pm aperture tube before estimating an average ingestion rate based on 4-6 h of feeding. A second similar set of feeding experiments using medium size larvae at 14 “C was set up to determine possible effects that larval crowding (0.5, 1, 2, 5, and 10 larvae - ml - ‘) may have on feeding rates. The first set of measurements were made using a known acceptable food level of 20 cells * ~1~ ‘, which represents 20 000 cells . larva ’ at a rearing density of 1 larva - ml - ‘. However, this meant that at high larval densities such as 10 ’ ml - 1 the amount of food available to indi~duals would be greatly reduced (to ~2000 cells *larva- ‘), making it more diflicult to separate the effect of crowding from effects due to possible food shortage. A second set of measurements was therefore made using food levels of 20000 cells available to each larva (i.e., at 0.5 larva +ml- I ration = 10 cells. ~1~ ‘, and at 10 larvae - ml- ’ ration = 200 cells * ~1~ I). METABOLIC
RATES
Oxygen consumption rates for several size groups of larvae were measured at 14 “C (20 I;rochuysis cells . pl- 1 and larval densities between 5 and 100 . ml - ’ ). Larvae were enclosed in a respiration chamber (206 ml) similar to that described by Bayne (197 I).
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A polarographic electrode coupled to a Strathkelvin 78 lb oxygen meter was mounted in the chamber and the amplifier output fed to a chart recorder. Water circulation in the chamber was provided by a 6-mm microstir bar driven at low speed by a submersible magnetic stirrer positioned under the chamber. Chamber and stirrer were immersed in a constant temperature ( + < 0.1 oC) water bath. Oxygen consumption not attributable to larvae was estimated in chambers without larvae over a 24-h period and a mean of 3.2 k 0.9 nl . h- 1 was subtracted from measured values. .4SSIMILATION
AND
GROWTH
EFFICIENCIES
As a separate component of a larger scallop project at the Pacific Biological Station Whyte (1987) and Whyte et al. (1987) determined the energy composition for the same .Zsochrysisspecies (4.23 kcal . g- ‘) and P. yesmensis larvae (1.78 kcal *g - ‘) used simultaneously in this study. Energy gained from ingestion (I) of Zsochrysis was estimated from feeding rates using an energy conversion factor of 1 cell = 0.690 pJ. Respiratory losses (R) were calculated from the exponential weight equation in Table I and converted to energy equivalents using 1 nl0, = 19.9 PJ (Elliott & Davidson, 1975). Energy spent on growth (G) was obtained from changes in shell length observed in Fig. 1 where l-pm increment = 45 ,uJ. The proportion of ingested food used for growth and respiration (referred to as assimilation efficiency (AE) (Crisp, 1975) was calculated as: AE = @ + ‘) x 100.
Z
The percentage of ingested ration converted to growth [referred to as gross growth efficiency (K,)] was estimated by: K, =
5x
100.
Z
The proportion of assimilated energy converted to growth [net growth efficiency (Z&)1 was calculated as: K, = ___
G
x 100.
(G + R) RESULTS
TEMPERATURE
AND
FOOD
CONCENTRATION
The mean shell lengths of P. yessoensis larvae reared at similar food levels increased as water temperatures were elevated (Fig. 1). Although growth rates were greatest at 18 ’ C survivorship was low resulting in the use of a standard rearing temperature of
B.A. MACDONALD
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z 14-15 “C, very similar to the rearing temperature of 13.2 “C suggested by Yoo (1969). A trend of faster growth rates at higher algal concentrations was observed, except at 10 “C where no further growth occurred in larvae reared at concentrations > 5
Fig. 1. Mean shell lengths plus 95% confidence intervals for P. yessoensis larvae reared (1 larva. ml - ‘) at three experimental temperatures (10, 14, and 18°C) and various concentrations (5-30 cells.pl-I) of Isochrysis cells.
cells * ~1~ ‘. Ingestion and filtration rates for three size classes of larvae measured under standard temperature and food conditions are presented in Fig. 2. Ingestion rate, expressed as the number of Isochrysis cells removed from suspension, was calculated as the change in particle concentration in experimental beakers over a known period 18’
14O /*\ p.1. .-.-& lo
PARTICLE
,:\.
----. --A----. 20
CONCENTRATION
30
to
(cells
20
30
~1 -’ )
Fig. 2. Estimated ingestion rates (cells. h- ‘) plus 95% confidence intervals and calculated filtration rates (~1. h- ‘) for small (A), medium (m), and large (0) P. yessoensb larvae (1 larva. ml- ‘) measured at three experimental temperatures (10, 14, and 18 “C) and various concentrations (5-30 cells. pl- ‘) of Isochrysis cells.
PHYSIOLOGICAL
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of time and divided by the number of larvae present. Food uptake was greater for larger larvae and at higher temperatures. Ingestion increased with food concentration at low levels but remained constant over a wide range of concentrations. Filtration rate, or volume of water cleared of particles per unit time, was calculated by dividing the ingestion rate by the appropriate particle concentration (Sprung, 1984b). Filtration rate declined steadily at higher food levels with the exception of the largest larvae, which showed maximum values at 10 (18 “C) and 15 ceils * fill l (14 “C). LARVAL DENSITY
When food concentration was held constant at 20 cells - /A- ’ ingestion rate declined rapidly at larval densities > 0.5-l - ml- ’ (Fig. 3). When food availability was increased proportionately to 20 000 cells - larva- I, ingestion declined from a maximum at 0.5 larva. ml- l, remained unchanged between 1 and 5 larvae * ml- *, then decreased to a
t 2
4
6
8
LARVAL
10 DENSITY
(ml“)
Fig. 3. Estimated ingestion rates (cells . h- ‘) plus 95% confidence intervals and calculated filtration rates (~1. h ’ ) for medium-size P. yemom& larvae measured at 14 “C, various larval densities (0.5-10 *ml - ’ ), and concentration of Zsochrysis cells of either 20 cells ‘~1~ ’ (0) or 20000 cells -larva- ’ (w).
minimum at 10 larvae - ml - ‘. Within the range of 1-5 larvae * ml - i, it may be possible to compensate for declining ingestion rates due to crowding simply by increasing food concentration. Filtration rates dropped dramatically as larval density increased from OS-2 larvae * ml- i. There was good agreement between these two feeding studies (20 cells . pl- ’ vs. 20 000 cells * larva- ‘) as indicated by the similar values at 1 larva * ml - ‘, where conditions were identical in each experiment. Larvae grown at a density of 2 * ml- ’ (and a ration level of 40 cells . ~1~ *) displayed the largest shell size (r 170 pm) at the end of the experiment (Fig. 4), but were still considerably smaller than larvae (Z 195 pm) grown at the same temperature, a lower food concentration (30 cells * ~1~ ‘) and at a density of only 1 larva - ml- ’ (Fig. 1).
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Initially larvae at 5 and 10 * ml- ’ grew at rates comparable to those of larvae at other densities, but once they reached r 150 pm growth slowed down and they all died by the end of Wk 3. -
180
I
160
5 2
140
E I -
!i
1 /
1
2
4
3
(weeks)
AGE
Fig. 4. Mean shell lengths plus 95% confidence intervals for P. yessoensir larvae reared at 14 “C, various larvaldensities(OS~ml~‘,O; 1~ml~*,~;2~ml~‘,A;5~ml-‘,0;and10~ml~’,O)andstandardfood concentration of 20000 Isochrysis cells 1larva- ‘. Note total mortality at 5 and 10 larvae. ml - ’ after 2-wk period.
OXYGEN CONSUMPTION
Equations describing relationships between oxygen consumption and shell length, total dry weight, and larval density are presented in Table I. Oxygen consumption rapidly declined as larval density increased (Fig. 5). Due to the suppression of 0, consumption at high larval densities, only values obtained at 5-20 larvae * ml - ’ were used to describe the relationships between $0, and shell length and total weight. It was impractical to measure oxygen consumption at larval densities < 5 - ml- ‘. When a small
I
200 600 800 400 TISSUE WEIGHT (ng)
25
DENSITY
, 50
I
75 ( l6rV6e
100 ml”)
Fig. 5. Oxygen consumption ($0, nl . h - ‘) rates for various sizes of P. yessoens3 larvae ( 150-900 ng total dry tissue weight). Also shown are rates measured at larval densities ranging from 5 to lOO*ml- i. Lines fitted to raw data represent predicted values from two power equations presented in Table I.
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YESSOENSrS LARVAE
(0.3-LO-ml) respiration chamber equipped with a microelectrode was used to measure the oxygen consumption of individual larvae, they appeared to remain inactive on the bottom, rendering measurements impossible. This apparent lack of activity may have been due to inadequate space for normal swimming behavior, although S. Siddall (pers. comm.) has observed active swimming in 160-pm Argopecten irradians larvae held in smaller containers. In his studies swimming performance appeared to be more dependent on the preexperiment treatment of the larvae. TABLE I Summary of parameters and coefficients of determination for regressions of oxygen consumption fy; $0,) against shell length (x; linear y = a + bx) and total dry weight (x; y = nxb) for P. yessoenris larvae measured at 14 “C. Power curve was also used to describe relationship between Vo, (y) and larval density (x).
ASSIMILATION
$0, vs. length
Vo, vs. weight
$0, vs. density
- 8.68 + (0.08x) (r’ = 0.81)
0.00087 x’.39 (r* = 0.82)
62.52 x - O.” (r* = 0.73)
AND GROWTH EFFICIENCIES
Estimates of energy acquired from feeding (Z) and energy spent on respiratory needs (R) and growth (G), together with assi~ation (AZ?) and growth efficiencies (K,, lu,) for different sizes of Pa~pec~e~ yessoensis larvae grown at 14 “C are presented in Table II. High assimilation efficiencies (> 70%) were observed for medium-size larvae at all three (higher) rations tested however, they decreased in small larvae as ration increased. Most ofthe assimilated energy was expended in respiration, leaving very little available for growth as indicated by the slow growth rates for P. yessoensis larvae and the low growth efficiencies (< 10%). Gross growth efficiencies for small larvae (141 pm) at low food concentrations were highest at 14 “C and lowest at 18 “C, but the opposite TABLE II Estimates of energy ingested (2, gJ *h- ‘) partitioned into respiratory losses (R, ,uJ 1h - ‘) and investments in growth (G, PJ . h - ‘) plus assimilation efliciency (AE, y. ) and gross (K, , ~~)/net (&, %) growth efficiencies for three sizes of P. yessue~ larvae. Larvae were reared under various concentrations of Is~c~ys~ aff galbana (T-RIO) at 14 “C. Note that growth efficiencies were not calculated for 245qm larvae because they did not reach this size during 4-wk growth experiment (see Fig. 1). Cells . pl- ’
141 pm (287 ng) R
I
44.9 44.9 44.9 44.9 44.9
34.1 68.3 99.0 95.6 102.4
G
AE
209 ,um (691 ng)
245 pm (904 ng) _.
K,
K,
R
I
G
AE
K,
K,
R
I
G
8.8 5.0 3.9 3.6 4.2
7.0 8.0 7.0 8.7
152.4 152.4 152.4 152.4 152.4
68.3 170.6 218.4 211.5 225.2
4.5 4.1 4.7 5.3
72 74 70
2.6 1.9 2.2 2.4
2.9 2.6 3.0 3.4
221.5 221.5 221.5 221.5 221.5
81.9 218.4 389.1 348.0 368.6
-
-5
IO 15 20 30
3.0 3.4 71 3.9 49 3.4 51 4.3 48
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at high food levels (Fig. 6). Medium-size larvae (209 pm) had higher K, values at 18 “C than at 14 “C. In most cases growth efficiency was independent of food concen~ation. was true
o
140
141pm .
10
20
PARTICLE
30
10
CONCENTRATION
20
(cells
pl“
30
1
Fig. 6. Estimates of gross growth efficieucy (K,) for three sizes of P. yessoe?& larvae reared at three expe~mental temperatures (10, 14, and 18 “C) and various concentrations of Zsochqwiv cells (5-30.@-‘).
The quantity of energy ingested did not exceed the amount required for respiration of small larvae at food concentrations < 6 cells * pl- ’ (Fig. 7). This critical food concentration increased to E 9 cells *pl- ’ for medium-size larvae and slightly > 10 cells - pl- ’ for large larvae (Table II).
200.
_
150-
k 7=
loo-
50.
5
lb
1’5
CELLS
2’0
3b
(p I-‘)
Fig. 7. Estimates of energy gained from ingestion (Z, @ *h - ‘) at various concentrations of isochryd cells (5-3O.pl- ‘) and energy required for respiration (R, ,u3. h- ‘) by small (0) and medium size (m) P. yessoemis larvae held at 14 “C.
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DISCUSSION FEEDING RESPONSE For many species, larval ingestion rates increase with particle concentration at low food levels, but become independent of concentration and may even decrease at high ration levels (Bayne, 1983). Feeding may be interrupted at higher concentrations because the gut system quickly tills and ingestion processes may be bypassed as in pseudofeces production by the adult (Crisp etal., 1985). Ingestion rates of 50-700 1~~hrysis cells * h - ’ and filtration rates between 3 and 45 ~1. h - ’ in P. yessoensis larvae are similar to values reported in the literature for veliger larvae of other species (for review, see Sprung, 1984b). Despite similarities in their feeding responses to increasing food concentrations, the larvae of mussels, oysters, and scallops differ in their energy requirements. Mussels are capable of gaining enough energy at low food levels (2 cells * pl- ‘) to meet respiratory and growth demands whereas oysters require a very high ration (> 50 cells - pl- ’ ; Crisp et al., 1985). Japanese scallop larvae apparently require between 6 and 10 cells * ~1~ I, making them intermediate between mussels and oysters. Sprung & Widdows (1986) using direct calorimetry described higher respiratory rates for M. edulis larvae than previously reported by Sprung (1984~). If these higher rates of respiration are now used to calculate the minimum food concentration necessary to sustain growth and respiratory demands a considerably higher estimate will result. It is interesting to note that at a concentration of 25 cells * pl- ’ (apparently low for oyster larvae and high for scallop larvae) 0. edulis ingests 300-400 cells. h- ’ (Crisp et al., 1985; Fig. 2), which is very similar to the ingestion estimates recorded here and by Yoo (1969) for P. yessoensis larvae at similar food concentrations. Scallop and mussel larvae may be more efficient than oyster larvae at low food concentrations, but are inefficient at the very dense concentrations that oysters apparently require. This may partially explain why large populations of adult pectinids are not normally found in turbid environments where many oyster species thrive. Tenore & Dunstan (1973) provide data on growth of small oysters (C. virginica), mussels (M. edulis), and scallops (Aequipecten irradians) held under identical conditions for 3 months, and found that scallops and mussels increased in dry weight by 60 and 49%, respectively, whereas oysters only increased 39%. DENSITYEFFECTS The decline in feeding rate at high densities of P. yessoensis larvae have also been reported for larvae of C. virginica(Fritz et al., 1984). These authors attributed a decrease in food uptake to heavier grazing rates that reduced food quantity below a level sufficient to sustain high feeding rates. In my study food levels were increased proportionately as larval density increased to maintain a constant ration for individual larvae. Ingestion rates still declined at higher larval densities possibly as a result of collisions due to overcrowding, which will interfere with feeding, or an accumulation of excretory pro-
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ducts, rather than as a consequence of a localized shortage of food cells. Ingestion rates may be maintained at high levels for P. yessoensis larvae held in rearing tanks at densities of l-5 - ml- ’ if food supply is mcreased proportionately. Short-term feeding studies suggested that ingestion rates were greatly reduced if larval densities exceeded 0.5 larvae -ml-‘. However, longer-term growth studies indicated that growth was not impaired until densities exceeded 2 larvae * ml- ‘. Below 2 larvae +ml- ‘, food concentration, not larval density, is the critical factor responsible for growth differences (Fig. 4). For example, at 2 larvae * ml- * food concentration was 40 cells *~1~ ’ while concentrations at 0.5 larvae * ml- ’ were equivalent to 10 cells * ,LLI-r. Malouf & Breese (1977) also reported faster growth at higher larval densities in one of their experiments {their Fig. 5) after food concentrations exceeded 140 cells - ,a- ‘. P. yexsoensis larvae held at higher densities of 5-10 - ml - ’ (100-200 cells - ~1~ ‘) appeared to grow at rates comparable to others at low densities early in the experiments but after reaching 150 ,um in length they suffered heavy mortality. Exposing Japanese scallop larvae to dense food concentrations may contribute to mortality just as signiticantly as rearing at high larval densities. Excessive formation of pseudofeces at high food levels may entangle or entrap larvae (Malouf & Breese, 1977). To determine the optimal rearing density and food concentration these factors and any possible interactions should be studied simultaneously. GROWTH
RATES
Growth rates of P. yessoensis larvae were positively correlated with increasing water temperatures within the natural range, in agreement with results reported for other species of molluscan larvae (Bayne, 1983). Greater ingestion rates apparently more than compensated for the presumed higher metabolic rates at warmer temperatures (18 “C), resulting in faster growth. Despite faster growth at the highest temperature (18 ‘C), survivorship is better at lower temperatures (14-15 ‘C) (N. Boume, pers. comm.) which is also true for A. C-radianslarvae (Tettelbach & Rhodes, 198 1). Growth is inhibited at low temperatures (10 “C) regardless of food availability. Only at the highest temperature, at which larvae were growing most rapidly, was the advantage associated with high food concen~ation clearly reflected in enhanced growth rates. Ingestion rates at medium to high food concentrations (15-20 cells * yl- ‘) were often equivalent to rates observed at the highest concentrations (30 cells * ~1~ ‘). This suggests that growth could be independent of food level at concentrations > 15 cells . PI- I. However, larvae grown in the densest algal suspension exhibited more rapid growth, revealing a discrepancy between predictions from short-term feeding studies and the results of long-term growth studies. Over a long period of time localized particle concentrations at intermediate food levels may drop below the concentration necessary to maintain rapid growth more often than at high food levels. This would result in more continuous exposure to good growth conditions at 30 cells * pl- ‘, leading to faster growth despite apparently similar ingestion rates. Alternatively, larvae may simply be more efficient at converting energy when it is readily or cont~uous~y available.
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Predictions based primarily on short-term feeding and respiratory studies that food concentrations between 6 and 10 Isoch~~is cells - PI- ’ are required to support metabolic demands are consistent with the results of long-term growth studies. For example growth at food concentrations below these levels (5 cells +pl- ‘) is clearly different from growth at higher concentrations. Just as food requirements increase with body size they probably increase with temperature. At 18 ’ C energy accumulation at 10 cells +~1~ ’ is inadequate to support good growth (Fig. l), but at 14 “C this ration supports growth equivalent to that observed at 20 cells *,d- I. However, at 18 oC and 5 cells - pl - ’ growth is equivalent to rates at 14 “C and 15 cells *pl- I. Survival and even growth at food levels below those required to meet respiratory demands is possible through a combination of very high absorption efficiency and utilization of energy reserves. M. eMis larvae can survive periods of 20-30 days (6-18 “C) without food and up to 150 days in sterilized seawater at 12 “C (Sprung, 1982). Although growth rates of htrval P. yessoensis reared only on ~soc~~sis appear slow compared with those of other bivalve larvae, they are similar to natural rates reported for this species. Larvae in Japan reach a shell length of 200 pm after 20 days growing under natural conditions at a rate of 5 pm * day - 1over a period of 30-47 days (Ventilla, 1982). Comparable shell lengths are achieved after 21 days at 18 “C and food concentrations of 20-30 cells * pl- ‘. P. yessoensis achieve shell lengths of 200 pm in 14 days when they are reared in the laboratory on a mixed algal diet (Thompson et al., 1985). However, the mean period of time required to reach this size was M24 days at 15 “C and 30-60 cells . ~1~ l. Other pectinid species such as Placopecten magellanicus achieve similar sizes in 13-23 days at 15 “C (Culliney, 1974) whereas Aequipecten (= Argopecten) i~r~d~~~ concen~~us grows to a length of 184 pm in 12 days at 24 “C (Sastry, 1965). EFFICIENCY
AND RESPIRATION
Values of assimilation efficiency for P. yessoensis larvae are similar to estimates obtained for M. edufis (Jespersen & Olsen, 1982) and 0. edulis (Crisp et al., 1985). The major difference between previous studies and this one is that most of the assimilated energy in the scallop larva is lost in respiration, whereas for the other species investment in growth represents a major component. Growth efficiencies of Japanese scallop larvae (< 10%) are much lower than those reported for other species, especially mussels and oysters which range from 17 to 80% (Sprung, 1984d; Crisp et al., 1985). Estimates of gross growth efficiency (K,) that exceed 40% seem unlikely when one considers absorption efficiency and the metabolic costs associated with activity and respiration. For example, estimates of absorption efficiency for 0. edulis larvae range from 21 to 52% (Gabbott & Holland, 1973) and from 15 to 45% (Walne, 1965). Sprung (1982) reported values of 18-44% for Mytihs edulis larvae, although gastropod larvae may have absorption efficiencies up to 60-70x (Pechenik, 1980). Very high values of K, observed at low food levels are probably overestimates because shell growth has occurred at the expense of energy reserves and energy conversions used are based on values recorded for well-fed larvae and not poorly fed larvae (Crisp et al., 1985).
168
B.A. MACDONALD
The oxygen consumption of Pa~~ec~n ye.womti larvae reached a rn~~urn of 13 nl . h- * +ind. - ’ and ranged from 13 to 29 ml O2 +g - l [AFDW] - h- ’ (assuming a figure of 60% ash for this species; Whyte et al., 1987). These values are higher than those reported for other veliger larvae varying from 1.6 to 10 ml 0, *g - ’ *h - I. High values (4.6-15.2 ml 0, *g - ’ *h - ‘) have also been reported for another species of pectinid, A. it-radians(S. Siddall, pers. comm.). Holland & Spencer (1973) reported values of 5-6 ml Oz. g- ’ *h- ’ for 0. edulis larvae based on biochemical changes during starvation, but this technique may produce minimal estimates of energy loss (Bayne, 1983). Whereas respiratory rates appear high in comparison to values for other bivalve larvae, P. ye~~oe~~i~larvae gain enough energy from feeding to exceed the respiratory cost at reasonably low food concen~ations (Fig. 7). The use of well-fed larvae could partially explain the higher metabolic rates observed in this study in contrast to the lower rates obtained for starved larvae in most of the other studies (M. Sprung, pers. comm.). Bivalve larvae migrate vertically at a rate of OS-7 mm - s- ’ and their activity may represent 8-50% of respiratory costs (Zeuthen, 1947; review in Sprung, 1984~). Rates of oxygen consumption are greatly reduced at high larval densities, probably as a result of collisions with other larvae, thereby interrupting swimming and/or feeding activity, or as a consequence of the accumulation of toxic excretory products (Walne, 1966; Millar & Scott, 1967). For example, respiratory rates decrease 35% as the density of P. yefsoensis larvae increases from 5 to 25 * ml - ’ (Fig. 5). Just as high larval density may cause inte~uptions in activity, any physical contact with the surfaces of the respiration chamber may also interfere with swim~ng, feeding or respiratory processes. In order to meaningfully integrate feeding and metabolic studies in bivalve larvae it is necessary to assess their response under realistic conditions, possibly concentrating on the food supply in natural seawater rather than only on artificial diets.
ACKNOWLEDGEMENTS
I would like to thank R. Thompson, S. Siddall, L. Fritz, N. Boume, and C, Hodgson for reviewing the typescript and W. Carosfeld, C. Hodgson, and D. Thompson for technical assistance and helpful discussions in the laboratory. A special thanks to M. Sprung for many helpful suggestions and to J. Whyte for giving me access to some of his unpublished data. While conducting this project at the Pacific Biological Station, Nanaimo, British Columbia, I was supported by a Canadian Government Visiting Postdoctoral Fellowship. New Jersey Agricultural Experiment Station Publication No. D-32001-1-88 supported by state funds. REFERENCES BAYNE,B. L., 1971.Oxygen consumption by three species of lameilibranch molluscs in declining ambient oxygen tension. Camp. Bioehem. Physiol., Vol. @A, pp. 955-970.
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ENERGETICS OF PATINOPECTEN
YESSOENSIS
LARVAE
169
B. L., 1983. Physiological ecology of marine molluscan larvae. In, The Mollusca, Vol. HI, edited by N.H. Verdonk et al., Academic Press, New York, New York, pp. 299-343. CRISP, D. J., 1975. The role of the pelagic larva. In, Perspectives in ex~~mentai allow, Vol. I, edited by P. Spencer Davis, Pergamon Press, Oxford, U.K., pp. 145-155. CRISP, D. J., A. B. YULE & K. N. WHITE, 1985. Feeding by oyster larvae: the functional response, energy budget and a comparison with mussel larvae. J. Mar. Biol. Assoc. U.K., Vol. 6S, pp. 759-783. CULLINEY,J. L., 1974. Larval development of the giant scallop Ptacopecten magetlanicus (@elin). Biol. Bull. (Woods Hole, Mass.), Vol. 147, pp. 321-332. DAVIS. H. C., 1953. On food and feeding of larvae of the American oyster, C. virginiica.Biol. Bull. (Woods Hole, Mass,), Vol. 104, pp. 334-350. ELLIOT, J. M. & W. DAVIDSON,1975. Energy equivalents of oxygen consumption in animal energetics. Oecologia (Berlin), Vol. 19, pp. 195-201. FRITZ, L. W., R.A. LUTZ, M. A. FOOTE, C. L. VAN DOVER & J. W. EWART, 1984. Selective feeding and grazing rates of oyster (Crassostrea virginica) larvae on natural phytoplankton assemblages. Estuaries, Vol. 7, pp. 513-518. GABBOXT,P. A. & D.L. HOLLAND,1973. Growth and metabolism of Ostrea eduhs larvae. Nature (London), Vol. 241, pp. 475-476. HOLLAND,D. L. & B.E. SPENCER,1973. Biochemical changes in fed and starved oysters, Ostrea edults L. during larval development, metamorphosis and early spat growth. f. Mar. Riot. Assoc. U.K., Vol. 53, pp. 287-298. JESPERSEN,H. & K. OLSEN, 1982. Bioenergetics in veliger larvae of Mytilus edulis L. Ophelia, Vol. 21, pp. 101-l 13. LOOSANOFF,V.L. & C.H. DAVIS, 1963. Rearing of bivalve mollusks. Adv. Mar. Biol., Vol. 1, pp. l-136. MALOUF, R.E. & W.P. BREESE, 1977. Food consumption and growth of larvae of the Pacific oyster, Cra.~sostrea gtgas (Thun~rg), in a constant flow rearing system. Proc. Nat. Sheath. Assoc., Vol. 67, pp. 7-16. MARU, K., 1972. [‘Morphological observations on the veliger larvae of a scallop Pattnopecten yessoensis (Jay).] Sci. Rep. Hokkaido Fish. Exp. Sm., No. 14, pp. 55-62 (In Japanese.) MILLAR, R. II. & J.M. SCOTT, 1967. The larvae of the oyster Ostrea edults during starvation J. Mar. Riot. Assoc. U.K., Vol. 47, pp. 475-484. MONET, M. G., 1979. A review of the fishery biology and culture of scallops. State Wash. Dep. Fish. Tech. Rep., No. 39, 100 pp. PECHENIR,J.A., 1980. Growth and energy balance during the larval lives of three prosobranch gastropods. J. Exp. Mar. Biol. Ecol., Vol. 44, pp. l-28. RIISGARD,H. U., A. RANDLOV& P. S. KRISTENSEN,1980. Rates of water processing, oxygen consumption and efficiency of particle retention in veligers and young post-metamorphic h4ytilu.redulis. Ophelia, Vol. 19, pp. 37-46. RIISGARD,H. U,, A. RANDLOV& K. HAMBURGER,1981. Oxygen consumption and clearance as a function of size in Mytjlus edulis L. veliger larvae. Opheita, Vol. 20, pp. 179-183. SASTRY,A. N., 1965. The development and external morphology of pelagic larval and post-larval stages of the bay scallop, Aequipecten irradians concentricus Say, reared in the laboratory. Bull. Mar. Sci., Vol. 15, pp. 417-435. SPRUNG, M., 1982. Untersuchungen zum Energiebudget der Larven der Miesmuschel, Mytilus eduh L. Dissertation, Universitat Kiel, Kiel, F.R.G., 146 pp. SPRUNG,M., 1984a. Physiolo~~al energetics of mussel larvae (Magi edultb). I. Shell growth and biomass. Mar. Ecol. Prog. Ser., Vol. 17, pp. 283-293. SPRUNG,M., 1984b. Physiological energetics of mussel larvae (Mytilus edutis). II. Food uptake. Mar. Ecoi. Prog. Ser., Vol. 17, pp. 295-305. SPRUNG,M., 1984c. Physiological energetics of mussel larvae (Mytilus edultk). III. Respiration. Mar, Ecol. Prog. Ser., Vol. 18, pp. 171-178. SPRUNG,M., 1984d. Physiological energetics of mussel larvae (Mytilus edults). IV. Efficiencies. Mar. EC~I. Prog. Ser., Vol. 18, pp. 179-186. SPRUNG,M. & J. WIDDOWS,1986. Rate of heat dissipation by gametes and larval stages ofMyti&s e&is. Mu,: Biof., Vol. 91, pp. 41-45. STRATHMANN,R. R., T. L. JAHN & J. R. C. FONSECA, 1972. Suspension feeding by marine invertebrate BAYNE,
170
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larvae: clearance of particles by ciliated bands of a rotifer, pluteus, and trochophore. Biol. Bull. (Woods Hole, Muss.), Vol. 142, pp. 505-519.
TENORE,K. R. & W. M. DUNSTAN,1973. Growth comparisons of oysters, mussels and scaHops cultivated on algae grown with artificial medium and treated sewage e&rent. Chesapeake Sci., Vol. 14, pp. 64-66. TETTELBACH,S.T. & E. W. RHODES, 1981. Combined effects of temperature and salinity on embryos and larvae of the northern bay scallop Argopecten irradians irradians. Mar. Biol., Vol. 63, pp. 249-256. THOMPSON,D., N. BOURNE& C. MANSON, 1987. Scallop breeding studies. In, 1983 and 1984 invertebrate management advice, Pacific region, edited by G. S. Jamieson, Can. M.S. Rep. Fish. Aquat. Sci., No. 1848, pp. 97-107. VEN~ILLA,R. F., 1982. The scallop industry in Japan. Adv. Mar. Biol., Vol. 20, pp. 309-382. WALNE, P.R., 1966. Experiments on the large scale culture of the larvae of Ostrea eduZis L. Ftih. Invest. Minist. Agric. Fish. Food. G. Br. Ser. ff Salmon Freshwater Fish., Vol. 25, pp. l-53. WHYTE,J. N. C., 1987. Biochemical composition and energy content of six species of phytoplankton used in mariculture of bivalves. Aquaculture. Vol. 60, pp. 23 1-241. WHYTE, J. N. C., N. BOURNE& C.A. HODGSON, 1987. Assessment of biochemical composition and energy reserves in larvae of the scallop Patinopecten yessoertsis. J. Exp. Mar. Biol. Ecol., Vol. 113, pp. 113-124. Yoo, S. K., 1969. [Food and growth ofcertain important bivalves.] Bull. Pusan F&h. Co&, Vol. 9, pp. 65-87. (In Korean.} ZEUTHEN, E., 1947. Body size and metabolic rate in the animal kingdom with special regard to marine microfauna. C.R. Trav. Lab. Carlsberg Ser. China., Vol. 26, pp. 17-161.
155
.JEM 01108
Physiological
energetics of Japanese scallop Patinopecten yessoensis larvae B.A. MacDonald
Rutgers ShellfTh Research Laboratory, Cook College, New Jersey Agricultural Experiment Station, Rutgers University, Port Norris, New Jersey. U.S.A. (Received
19 January
1988; revision
received
3 May 1988; accepted
7 May 1988)
Growth and ingestion rates were determined for Japanese scallop Patinopecten yessoensis larvae reared at temperatures between 10 and 18 “C and fed concentrations of Isochrysis aK galbana (clone T-ISO) cells between 5 and 30 cells . ply ’ to gain insight into energy balance. Veliger larvae were held in experimental chambers at densities of 0.5-100. ml ’ to assess the influence of crowding on growth, respiratory and feeding rates. Long-term growth studies lasting 28 days indicated that growth was most rapid at highest food concentrations of 30 cells . pl_ ’ despite indications from short-term feeding studies that ingestion was at a maximum and independent ofconcentration between 15 and 30 cells. ~1~ ‘. Growth and ingestion are both reduced as the density of larvae increases. Feeding rates (6 h) remained fairly constant between densities of l-5 larvae ml- ’ if food availability was increased proportionately. However, growth experiments lasting 28 days revealed extremely low survivorship if larvae are reared at densities of > 2 ml _ ‘. Respiratory rates were higher than previously reported for bivalve larvae and reaching values of 13 nl . h- ’ or 13-29 ml ~35% at larval densities between 5 and 0, g ’ [AFDW] h - ‘. Oxygen consumption was reduced 25 . ml ’ which are typical densities used when measuring metabolic rates of veliger larvae. Assimilation efficiencies between = 55 and 80% were comparable to published values for mussel and oyster larvae but higher respiratory demand and comparatively slow growth rates for this species were reflected in lower growth effkiencies than those previously reported for bivalve larvae. Japanese scallop larvae apparently require a minimum food concentration of 7-15 cells. ~1~ ’ (depending on size) to gain sufficient energy to support respiration and growth. Despite morphological similarities between species of bivalve larvae they may differ in their rates of energy acquisition and utilization. Abstract:
Key words: Energetics;
Feeding;
Growth;
Larva;
Respiration;
Scallop
INTRODUCTION
Planktotrophic marine larvae meet their nutritional requirements by filtering particulate material, primarily microalgae from the surrounding seawater, with the ciliated velum (Strathmann et al., 1972). Aspects of larval feeding behavior that vary in response to environmental conditions are of fundamental interest to physiological ecologists studying energy acquisition and utilization and are highly relevant to commercial hatcheries (Bayne, 1983). Energy intake has usually been determined by measuring
Contribution 734 from Marine Sciences Research Laboratory. Correspondence address: B.A. MacDonald, Marine Sciences Research of Newfoundland, St. John’s, Newfoundland AlC 5S7, Canada. 0022-0981/88/$03.50
0 1988 Elsevier
Science
Publishers
Laboratory,
B.V. (Biomedical
Division)
Memorial
University
156
B.A. MACDONALD
ingestion or filtration rates over short periods of time, and estimates of the energy requirements of feeding or swimming obtained by measuring rates of oxygen consumption using a variety of techniques (Sprung, 1984~). Long-term changes in growth and survival have been used as indicators of larval response to a range of environmental or hatchery conditions, because such changes represent the net result of all integrated physiological processes within the organism. Most of the information available on growth rates and feeding characteristics of molluscan larvae has been provided by studies on commercially important species grown in hatcheries at artificially high food levels. Feeding characteristics of larvae reared at ambient temperatures, a variety of food levels, including the low concentrations normally found in the natural environment, have recently been described for Mytilus edulis and Ostrea edulis (Sprung, 1984b; Crisp et al., 1985). The basic feeding response to increasing food concentrations exhibited by larvae in these studies was for ingestion to increase until reaching a plateau while filtration rate decreased steadily. Comparative studies such as these have revealed major differences in the energy requirements of oyster and mussel larvae, and suggest that the latter are capable of growing at food levels far lower than those required by the former (Crisp et al., 1985). A problem encountered when studying larvae is the need to enclose and concentrate them in order to detect measurable changes in feeding or metabolic rates over a short period (Sprung, 1984~). Larval densities in experimental containers have ranged from 1 to 100*mll (Walne 1966; Millar & Scott, 1967; Riisgkd et al., 1980, 1981; Fritz et al., 1984; Sprung, 1984a; Crisp et al., 1985; this study). Natural larval densities are obviously much lower, with maximum densities approaching 1200 * m - 3 or 0.0012. ml- ’ for Patinopecten yessoensis (Ventilla, 1982) and a mean of 0.002. ml ’ for Crassostrea virginica (Fritz et al., 1984). Reductions in feeding rate (Fritz et al., 1984) growth rate (Davis, 1953; Loosanoff & Davis, 1963; Malouf & Breese, 1977), and metabolic rate (Walne, 1966; Millar & Scott, 1967) have all been reported for bivalve larvae at greater densities. The degree of concentration could have a profound effect on larval behavior by greatly increasing the likelihood of one individual colliding with another, causing damage or an interruption in feeding activity, and by increasing the concentration of excretory products. Interpreting results obtained with dense cultures is rather difficult, and recent studies suggest that larval density is a factor worth considering. The Japanese scallop industry (P. yessoensis) represents a major portion of the world’s total scallop production and is currently supported by an extensive program to monitor natural larval abundances and spat collection (Mottet, 1979; Ventilla, 1982). Declines in several natural scallop fisheries, high market demand, and the success of the Japanese industry have prompted recent international interest in the potential benefits of culturing scallops. Insufficient or irregular natural recruitment for pectinids in several areas has resulted in studies on the feasibility of commercial-scale scallop hatcheries like those existing for oysters. In this study the rates of feeding, metabolism, and growth of larval P. yessoensis were
PHYSIOLO~ICALENERGETICS OF PATZ~~PECT~~YESSOE~SZS
LARVAE
157
determined at food levels, temperatures, and larval densities appropriate to natural conditions and those encountered in hatcheries. The objectives of this study were to assess the energy requirements of larvae and to determine conditions for optimal growth. Comparisons will be made between conditions predicted to be optimal based on short-term feeding studies and those found to give the best results based on long-term growth studies.
MATERIALS AND METHODS SPAWNING AND REARING
Broodstock Japanese scallops F. yes.roe&s were held in quarantine and kept in spawning condition by holding them for at least 1 wk in 5-8 “C seawater and feeding them a mixture of Zsochrysis aff. galbana, Chaetoceros calcitrans, and Thalassiosira pseudonana. The following brief description of spawning and rearing conditions was taken from Thompson et al. (1985). Scallops were induced to spawn by removing them from seawater for R 1 h before being returned to water warmed to 12 or 15 “C or by an injection of 0.4 ml of 2 x 10W5M solution of serotonin into the adductor muscle. After the addition of sperm, fertilized eggs were gently washed and placed in seawater ( 14 ’ C) at a concen~ation of 4-l 1 eggs * ml - ’ and allowed to develop into trochophore (l-2 days) and veliger larvae (2-3 days). Developm~t~ stages and growth rates of P. yessoensis larvae in the natural environment have been provided by Maru (1972) and Ventilla (1982) (see Discussion). Larvae in this study achieved a mean shell length (D stage) of Q 120 pm ( RZ145 ng) 3 days after fertilization. These larvae metamorphosed x 30 days after fertilization when they reached a mean shell length of 250-260 pm and weighed between 900 and 1000 ng (Thompson et al., 1985; Whyte et al., 1987). Larvae were reared at a density of 1-2*ml- ’ in large fiberglass cylinders (0.35-6 m3) with a complete water exchange (15 “C) every 3-4 days. GROWTH
RATES
Larvae from the same large rearing tank (3 days old) were held at a density of 1 ind . ml - ’ in 4-l glass beakers cont~~g 3.5 1 of filtered seawater (1 pm) at ambient salinity (29 + 1“/,), and were fed exclusively on ZsochrySs af?‘.galbana (clone T-ISO) at concentrations of 5, 10, 15, 20, and 30 cells * ~1~ *. The influence of crowding was determined by maintaining food availability at 20 000 cells * larva- ’ while varying larval density (0.5, 1,2, 5, and 10 larvae *ml- ‘. Three replicate beakers were set up for each experimental treatment and placed in water baths at either 10, 14, or 18 “C. To keep food particles in suspension, each beaker was supplied with air from a line fitted with a glass pipette at the end to deliver small bubbles to the bottom of the chamber at rate of 1-2 bubbles * s - I. Particle counts were monitored frequently using a Coulter TAIr counter and adjusted if they varied by > 10% from original levels.
B.A. MACDONALD
158
Every 2-3 days larvae were concentrated on a 53-pm screen and resuspended in filtered water in a clean beaker. Once a week during routine water changes larvae were examined under a microscope equipped with a calibrated eyepiece graticule, and shell length ( it 5 pm) determined for 30 larvae selected at random in each replicate. Total dry weight and ash free dry weight were determined for various sizes of surplus groups of larvae after washing with distilled water and collecting them under vacuum on preashed and preweighed fiber glass filters (GF/C; 21 mm diameter). Filters were dried at 90 “C for several hours, weighed on an ultramicrobalance to & 1 pg, and then placed in a muffle furnace at 500 “C for 48 h before determining final ash weight. FEEDING
RATES
Larvae from one of three standardized size classes [mean shell length, small x 140 ,um (125-170 pm), medium z 200 pm (160-230 pm), large x 240 pm (200-270 pm)] were added (1 * ml- ‘) to 2-l glass beakers containing 1.8 1 of filtered seawater ( -=z1 pm). While the larvae used for growth studies were from the same batch those individuals used for short-term feeding and metabolic studies were from different batches that had received similar treatment. Three experimental and one control beaker (without larvae) were set up with aeration and placed in water baths at either 10, 14, or 18 “C at each of the following concentrations: 5, 10, 15,20, and 30 cells * pl- r. The use of control beakers made it possible to determine whether changes in particle counts were unrelated to larval feeding, such as cells dividing or settling, and whether the smallest larvae were feeding at all. After an initial adjustment period of z 2 h, 25 ml samples were removed from each beaker every 30-60 min and passed through a 53-pm screen to remove larvae. Isochrysis cells were counted five times for each sample using a Coulter TA,, counter fitted with a 50-pm aperture tube before estimating an average ingestion rate based on 4-6 h of feeding. A second similar set of feeding experiments using medium size larvae at 14 “C was set up to determine possible effects that larval crowding (0.5, 1, 2, 5, and 10 larvae - ml - ‘) may have on feeding rates. The first set of measurements were made using a known acceptable food level of 20 cells * ~1~ ‘, which represents 20 000 cells . larva ’ at a rearing density of 1 larva - ml - ‘. However, this meant that at high larval densities such as 10 ’ ml - 1 the amount of food available to indi~duals would be greatly reduced (to ~2000 cells *larva- ‘), making it more diflicult to separate the effect of crowding from effects due to possible food shortage. A second set of measurements was therefore made using food levels of 20000 cells available to each larva (i.e., at 0.5 larva +ml- I ration = 10 cells. ~1~ ‘, and at 10 larvae - ml- ’ ration = 200 cells * ~1~ I). METABOLIC
RATES
Oxygen consumption rates for several size groups of larvae were measured at 14 “C (20 I;rochuysis cells . pl- 1 and larval densities between 5 and 100 . ml - ’ ). Larvae were enclosed in a respiration chamber (206 ml) similar to that described by Bayne (197 I).
PHYSIOLOGICAL
ENERGETICS
OF PATZNOPECTEN
YESSOENSZS
LARVAE
159
A polarographic electrode coupled to a Strathkelvin 78 lb oxygen meter was mounted in the chamber and the amplifier output fed to a chart recorder. Water circulation in the chamber was provided by a 6-mm microstir bar driven at low speed by a submersible magnetic stirrer positioned under the chamber. Chamber and stirrer were immersed in a constant temperature ( + < 0.1 oC) water bath. Oxygen consumption not attributable to larvae was estimated in chambers without larvae over a 24-h period and a mean of 3.2 k 0.9 nl . h- 1 was subtracted from measured values. .4SSIMILATION
AND
GROWTH
EFFICIENCIES
As a separate component of a larger scallop project at the Pacific Biological Station Whyte (1987) and Whyte et al. (1987) determined the energy composition for the same .Zsochrysisspecies (4.23 kcal . g- ‘) and P. yesmensis larvae (1.78 kcal *g - ‘) used simultaneously in this study. Energy gained from ingestion (I) of Zsochrysis was estimated from feeding rates using an energy conversion factor of 1 cell = 0.690 pJ. Respiratory losses (R) were calculated from the exponential weight equation in Table I and converted to energy equivalents using 1 nl0, = 19.9 PJ (Elliott & Davidson, 1975). Energy spent on growth (G) was obtained from changes in shell length observed in Fig. 1 where l-pm increment = 45 ,uJ. The proportion of ingested food used for growth and respiration (referred to as assimilation efficiency (AE) (Crisp, 1975) was calculated as: AE = @ + ‘) x 100.
Z
The percentage of ingested ration converted to growth [referred to as gross growth efficiency (K,)] was estimated by: K, =
5x
100.
Z
The proportion of assimilated energy converted to growth [net growth efficiency (Z&)1 was calculated as: K, = ___
G
x 100.
(G + R) RESULTS
TEMPERATURE
AND
FOOD
CONCENTRATION
The mean shell lengths of P. yessoensis larvae reared at similar food levels increased as water temperatures were elevated (Fig. 1). Although growth rates were greatest at 18 ’ C survivorship was low resulting in the use of a standard rearing temperature of
B.A. MACDONALD
160
z 14-15 “C, very similar to the rearing temperature of 13.2 “C suggested by Yoo (1969). A trend of faster growth rates at higher algal concentrations was observed, except at 10 “C where no further growth occurred in larvae reared at concentrations > 5
Fig. 1. Mean shell lengths plus 95% confidence intervals for P. yessoensis larvae reared (1 larva. ml - ‘) at three experimental temperatures (10, 14, and 18°C) and various concentrations (5-30 cells.pl-I) of Isochrysis cells.
cells * ~1~ ‘. Ingestion and filtration rates for three size classes of larvae measured under standard temperature and food conditions are presented in Fig. 2. Ingestion rate, expressed as the number of Isochrysis cells removed from suspension, was calculated as the change in particle concentration in experimental beakers over a known period 18’
14O /*\ p.1. .-.-& lo
PARTICLE
,:\.
----. --A----. 20
CONCENTRATION
30
to
(cells
20
30
~1 -’ )
Fig. 2. Estimated ingestion rates (cells. h- ‘) plus 95% confidence intervals and calculated filtration rates (~1. h- ‘) for small (A), medium (m), and large (0) P. yessoensb larvae (1 larva. ml- ‘) measured at three experimental temperatures (10, 14, and 18 “C) and various concentrations (5-30 cells. pl- ‘) of Isochrysis cells.
PHYSIOLOGICAL
ENERGETICS OF PAXINOPECTEN
YESSOENSIS
LARVAE
161
of time and divided by the number of larvae present. Food uptake was greater for larger larvae and at higher temperatures. Ingestion increased with food concentration at low levels but remained constant over a wide range of concentrations. Filtration rate, or volume of water cleared of particles per unit time, was calculated by dividing the ingestion rate by the appropriate particle concentration (Sprung, 1984b). Filtration rate declined steadily at higher food levels with the exception of the largest larvae, which showed maximum values at 10 (18 “C) and 15 ceils * fill l (14 “C). LARVAL DENSITY
When food concentration was held constant at 20 cells - /A- ’ ingestion rate declined rapidly at larval densities > 0.5-l - ml- ’ (Fig. 3). When food availability was increased proportionately to 20 000 cells - larva- I, ingestion declined from a maximum at 0.5 larva. ml- l, remained unchanged between 1 and 5 larvae * ml- *, then decreased to a
t 2
4
6
8
LARVAL
10 DENSITY
(ml“)
Fig. 3. Estimated ingestion rates (cells . h- ‘) plus 95% confidence intervals and calculated filtration rates (~1. h ’ ) for medium-size P. yemom& larvae measured at 14 “C, various larval densities (0.5-10 *ml - ’ ), and concentration of Zsochrysis cells of either 20 cells ‘~1~ ’ (0) or 20000 cells -larva- ’ (w).
minimum at 10 larvae - ml - ‘. Within the range of 1-5 larvae * ml - i, it may be possible to compensate for declining ingestion rates due to crowding simply by increasing food concentration. Filtration rates dropped dramatically as larval density increased from OS-2 larvae * ml- i. There was good agreement between these two feeding studies (20 cells . pl- ’ vs. 20 000 cells * larva- ‘) as indicated by the similar values at 1 larva * ml - ‘, where conditions were identical in each experiment. Larvae grown at a density of 2 * ml- ’ (and a ration level of 40 cells . ~1~ *) displayed the largest shell size (r 170 pm) at the end of the experiment (Fig. 4), but were still considerably smaller than larvae (Z 195 pm) grown at the same temperature, a lower food concentration (30 cells * ~1~ ‘) and at a density of only 1 larva - ml- ’ (Fig. 1).
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162
Initially larvae at 5 and 10 * ml- ’ grew at rates comparable to those of larvae at other densities, but once they reached r 150 pm growth slowed down and they all died by the end of Wk 3. -
180
I
160
5 2
140
E I -
!i
1 /
1
2
4
3
(weeks)
AGE
Fig. 4. Mean shell lengths plus 95% confidence intervals for P. yessoensir larvae reared at 14 “C, various larvaldensities(OS~ml~‘,O; 1~ml~*,~;2~ml~‘,A;5~ml-‘,0;and10~ml~’,O)andstandardfood concentration of 20000 Isochrysis cells 1larva- ‘. Note total mortality at 5 and 10 larvae. ml - ’ after 2-wk period.
OXYGEN CONSUMPTION
Equations describing relationships between oxygen consumption and shell length, total dry weight, and larval density are presented in Table I. Oxygen consumption rapidly declined as larval density increased (Fig. 5). Due to the suppression of 0, consumption at high larval densities, only values obtained at 5-20 larvae * ml - ’ were used to describe the relationships between $0, and shell length and total weight. It was impractical to measure oxygen consumption at larval densities < 5 - ml- ‘. When a small
I
200 600 800 400 TISSUE WEIGHT (ng)
25
DENSITY
, 50
I
75 ( l6rV6e
100 ml”)
Fig. 5. Oxygen consumption ($0, nl . h - ‘) rates for various sizes of P. yessoens3 larvae ( 150-900 ng total dry tissue weight). Also shown are rates measured at larval densities ranging from 5 to lOO*ml- i. Lines fitted to raw data represent predicted values from two power equations presented in Table I.
PHYSIOLOGICAL
ENERGETICS OF PAT~~~PECTE~
163
YESSOENSrS LARVAE
(0.3-LO-ml) respiration chamber equipped with a microelectrode was used to measure the oxygen consumption of individual larvae, they appeared to remain inactive on the bottom, rendering measurements impossible. This apparent lack of activity may have been due to inadequate space for normal swimming behavior, although S. Siddall (pers. comm.) has observed active swimming in 160-pm Argopecten irradians larvae held in smaller containers. In his studies swimming performance appeared to be more dependent on the preexperiment treatment of the larvae. TABLE I Summary of parameters and coefficients of determination for regressions of oxygen consumption fy; $0,) against shell length (x; linear y = a + bx) and total dry weight (x; y = nxb) for P. yessoenris larvae measured at 14 “C. Power curve was also used to describe relationship between Vo, (y) and larval density (x).
ASSIMILATION
$0, vs. length
Vo, vs. weight
$0, vs. density
- 8.68 + (0.08x) (r’ = 0.81)
0.00087 x’.39 (r* = 0.82)
62.52 x - O.” (r* = 0.73)
AND GROWTH EFFICIENCIES
Estimates of energy acquired from feeding (Z) and energy spent on respiratory needs (R) and growth (G), together with assi~ation (AZ?) and growth efficiencies (K,, lu,) for different sizes of Pa~pec~e~ yessoensis larvae grown at 14 “C are presented in Table II. High assimilation efficiencies (> 70%) were observed for medium-size larvae at all three (higher) rations tested however, they decreased in small larvae as ration increased. Most ofthe assimilated energy was expended in respiration, leaving very little available for growth as indicated by the slow growth rates for P. yessoensis larvae and the low growth efficiencies (< 10%). Gross growth efficiencies for small larvae (141 pm) at low food concentrations were highest at 14 “C and lowest at 18 “C, but the opposite TABLE II Estimates of energy ingested (2, gJ *h- ‘) partitioned into respiratory losses (R, ,uJ 1h - ‘) and investments in growth (G, PJ . h - ‘) plus assimilation efliciency (AE, y. ) and gross (K, , ~~)/net (&, %) growth efficiencies for three sizes of P. yessue~ larvae. Larvae were reared under various concentrations of Is~c~ys~ aff galbana (T-RIO) at 14 “C. Note that growth efficiencies were not calculated for 245qm larvae because they did not reach this size during 4-wk growth experiment (see Fig. 1). Cells . pl- ’
141 pm (287 ng) R
I
44.9 44.9 44.9 44.9 44.9
34.1 68.3 99.0 95.6 102.4
G
AE
209 ,um (691 ng)
245 pm (904 ng) _.
K,
K,
R
I
G
AE
K,
K,
R
I
G
8.8 5.0 3.9 3.6 4.2
7.0 8.0 7.0 8.7
152.4 152.4 152.4 152.4 152.4
68.3 170.6 218.4 211.5 225.2
4.5 4.1 4.7 5.3
72 74 70
2.6 1.9 2.2 2.4
2.9 2.6 3.0 3.4
221.5 221.5 221.5 221.5 221.5
81.9 218.4 389.1 348.0 368.6
-
-5
IO 15 20 30
3.0 3.4 71 3.9 49 3.4 51 4.3 48
B.A. MACDONALD
164
at high food levels (Fig. 6). Medium-size larvae (209 pm) had higher K, values at 18 “C than at 14 “C. In most cases growth efficiency was independent of food concen~ation. was true
o
140
141pm .
10
20
PARTICLE
30
10
CONCENTRATION
20
(cells
pl“
30
1
Fig. 6. Estimates of gross growth efficieucy (K,) for three sizes of P. yessoe?& larvae reared at three expe~mental temperatures (10, 14, and 18 “C) and various concentrations of Zsochqwiv cells (5-30.@-‘).
The quantity of energy ingested did not exceed the amount required for respiration of small larvae at food concentrations < 6 cells * pl- ’ (Fig. 7). This critical food concentration increased to E 9 cells *pl- ’ for medium-size larvae and slightly > 10 cells - pl- ’ for large larvae (Table II).
200.
_
150-
k 7=
loo-
50.
5
lb
1’5
CELLS
2’0
3b
(p I-‘)
Fig. 7. Estimates of energy gained from ingestion (Z, @ *h - ‘) at various concentrations of isochryd cells (5-3O.pl- ‘) and energy required for respiration (R, ,u3. h- ‘) by small (0) and medium size (m) P. yessoemis larvae held at 14 “C.
PHYSIOLOGICALENERGETICSOF PATINOPECTEN YESSOENSISLARVAE
165
DISCUSSION FEEDING RESPONSE For many species, larval ingestion rates increase with particle concentration at low food levels, but become independent of concentration and may even decrease at high ration levels (Bayne, 1983). Feeding may be interrupted at higher concentrations because the gut system quickly tills and ingestion processes may be bypassed as in pseudofeces production by the adult (Crisp etal., 1985). Ingestion rates of 50-700 1~~hrysis cells * h - ’ and filtration rates between 3 and 45 ~1. h - ’ in P. yessoensis larvae are similar to values reported in the literature for veliger larvae of other species (for review, see Sprung, 1984b). Despite similarities in their feeding responses to increasing food concentrations, the larvae of mussels, oysters, and scallops differ in their energy requirements. Mussels are capable of gaining enough energy at low food levels (2 cells * pl- ‘) to meet respiratory and growth demands whereas oysters require a very high ration (> 50 cells - pl- ’ ; Crisp et al., 1985). Japanese scallop larvae apparently require between 6 and 10 cells * ~1~ I, making them intermediate between mussels and oysters. Sprung & Widdows (1986) using direct calorimetry described higher respiratory rates for M. edulis larvae than previously reported by Sprung (1984~). If these higher rates of respiration are now used to calculate the minimum food concentration necessary to sustain growth and respiratory demands a considerably higher estimate will result. It is interesting to note that at a concentration of 25 cells * pl- ’ (apparently low for oyster larvae and high for scallop larvae) 0. edulis ingests 300-400 cells. h- ’ (Crisp et al., 1985; Fig. 2), which is very similar to the ingestion estimates recorded here and by Yoo (1969) for P. yessoensis larvae at similar food concentrations. Scallop and mussel larvae may be more efficient than oyster larvae at low food concentrations, but are inefficient at the very dense concentrations that oysters apparently require. This may partially explain why large populations of adult pectinids are not normally found in turbid environments where many oyster species thrive. Tenore & Dunstan (1973) provide data on growth of small oysters (C. virginica), mussels (M. edulis), and scallops (Aequipecten irradians) held under identical conditions for 3 months, and found that scallops and mussels increased in dry weight by 60 and 49%, respectively, whereas oysters only increased 39%. DENSITYEFFECTS The decline in feeding rate at high densities of P. yessoensis larvae have also been reported for larvae of C. virginica(Fritz et al., 1984). These authors attributed a decrease in food uptake to heavier grazing rates that reduced food quantity below a level sufficient to sustain high feeding rates. In my study food levels were increased proportionately as larval density increased to maintain a constant ration for individual larvae. Ingestion rates still declined at higher larval densities possibly as a result of collisions due to overcrowding, which will interfere with feeding, or an accumulation of excretory pro-
B.A. MACDONALD
166
ducts, rather than as a consequence of a localized shortage of food cells. Ingestion rates may be maintained at high levels for P. yessoensis larvae held in rearing tanks at densities of l-5 - ml- ’ if food supply is mcreased proportionately. Short-term feeding studies suggested that ingestion rates were greatly reduced if larval densities exceeded 0.5 larvae -ml-‘. However, longer-term growth studies indicated that growth was not impaired until densities exceeded 2 larvae * ml- ‘. Below 2 larvae +ml- ‘, food concentration, not larval density, is the critical factor responsible for growth differences (Fig. 4). For example, at 2 larvae * ml- * food concentration was 40 cells *~1~ ’ while concentrations at 0.5 larvae * ml- ’ were equivalent to 10 cells * ,LLI-r. Malouf & Breese (1977) also reported faster growth at higher larval densities in one of their experiments {their Fig. 5) after food concentrations exceeded 140 cells - ,a- ‘. P. yexsoensis larvae held at higher densities of 5-10 - ml - ’ (100-200 cells - ~1~ ‘) appeared to grow at rates comparable to others at low densities early in the experiments but after reaching 150 ,um in length they suffered heavy mortality. Exposing Japanese scallop larvae to dense food concentrations may contribute to mortality just as signiticantly as rearing at high larval densities. Excessive formation of pseudofeces at high food levels may entangle or entrap larvae (Malouf & Breese, 1977). To determine the optimal rearing density and food concentration these factors and any possible interactions should be studied simultaneously. GROWTH
RATES
Growth rates of P. yessoensis larvae were positively correlated with increasing water temperatures within the natural range, in agreement with results reported for other species of molluscan larvae (Bayne, 1983). Greater ingestion rates apparently more than compensated for the presumed higher metabolic rates at warmer temperatures (18 “C), resulting in faster growth. Despite faster growth at the highest temperature (18 ‘C), survivorship is better at lower temperatures (14-15 ‘C) (N. Boume, pers. comm.) which is also true for A. C-radianslarvae (Tettelbach & Rhodes, 198 1). Growth is inhibited at low temperatures (10 “C) regardless of food availability. Only at the highest temperature, at which larvae were growing most rapidly, was the advantage associated with high food concen~ation clearly reflected in enhanced growth rates. Ingestion rates at medium to high food concentrations (15-20 cells * yl- ‘) were often equivalent to rates observed at the highest concentrations (30 cells * ~1~ ‘). This suggests that growth could be independent of food level at concentrations > 15 cells . PI- I. However, larvae grown in the densest algal suspension exhibited more rapid growth, revealing a discrepancy between predictions from short-term feeding studies and the results of long-term growth studies. Over a long period of time localized particle concentrations at intermediate food levels may drop below the concentration necessary to maintain rapid growth more often than at high food levels. This would result in more continuous exposure to good growth conditions at 30 cells * pl- ‘, leading to faster growth despite apparently similar ingestion rates. Alternatively, larvae may simply be more efficient at converting energy when it is readily or cont~uous~y available.
PHYSIOLOGICAL
ENERGETICS
OF PATINOPECTEN
YESSOENSIS
LARVAE
167
Predictions based primarily on short-term feeding and respiratory studies that food concentrations between 6 and 10 Isoch~~is cells - PI- ’ are required to support metabolic demands are consistent with the results of long-term growth studies. For example growth at food concentrations below these levels (5 cells +pl- ‘) is clearly different from growth at higher concentrations. Just as food requirements increase with body size they probably increase with temperature. At 18 ’ C energy accumulation at 10 cells +~1~ ’ is inadequate to support good growth (Fig. l), but at 14 “C this ration supports growth equivalent to that observed at 20 cells *,d- I. However, at 18 oC and 5 cells - pl - ’ growth is equivalent to rates at 14 “C and 15 cells *pl- I. Survival and even growth at food levels below those required to meet respiratory demands is possible through a combination of very high absorption efficiency and utilization of energy reserves. M. eMis larvae can survive periods of 20-30 days (6-18 “C) without food and up to 150 days in sterilized seawater at 12 “C (Sprung, 1982). Although growth rates of htrval P. yessoensis reared only on ~soc~~sis appear slow compared with those of other bivalve larvae, they are similar to natural rates reported for this species. Larvae in Japan reach a shell length of 200 pm after 20 days growing under natural conditions at a rate of 5 pm * day - 1over a period of 30-47 days (Ventilla, 1982). Comparable shell lengths are achieved after 21 days at 18 “C and food concentrations of 20-30 cells * pl- ‘. P. yessoensis achieve shell lengths of 200 pm in 14 days when they are reared in the laboratory on a mixed algal diet (Thompson et al., 1985). However, the mean period of time required to reach this size was M24 days at 15 “C and 30-60 cells . ~1~ l. Other pectinid species such as Placopecten magellanicus achieve similar sizes in 13-23 days at 15 “C (Culliney, 1974) whereas Aequipecten (= Argopecten) i~r~d~~~ concen~~us grows to a length of 184 pm in 12 days at 24 “C (Sastry, 1965). EFFICIENCY
AND RESPIRATION
Values of assimilation efficiency for P. yessoensis larvae are similar to estimates obtained for M. edufis (Jespersen & Olsen, 1982) and 0. edulis (Crisp et al., 1985). The major difference between previous studies and this one is that most of the assimilated energy in the scallop larva is lost in respiration, whereas for the other species investment in growth represents a major component. Growth efficiencies of Japanese scallop larvae (< 10%) are much lower than those reported for other species, especially mussels and oysters which range from 17 to 80% (Sprung, 1984d; Crisp et al., 1985). Estimates of gross growth efficiency (K,) that exceed 40% seem unlikely when one considers absorption efficiency and the metabolic costs associated with activity and respiration. For example, estimates of absorption efficiency for 0. edulis larvae range from 21 to 52% (Gabbott & Holland, 1973) and from 15 to 45% (Walne, 1965). Sprung (1982) reported values of 18-44% for Mytihs edulis larvae, although gastropod larvae may have absorption efficiencies up to 60-70x (Pechenik, 1980). Very high values of K, observed at low food levels are probably overestimates because shell growth has occurred at the expense of energy reserves and energy conversions used are based on values recorded for well-fed larvae and not poorly fed larvae (Crisp et al., 1985).
168
B.A. MACDONALD
The oxygen consumption of Pa~~ec~n ye.womti larvae reached a rn~~urn of 13 nl . h- * +ind. - ’ and ranged from 13 to 29 ml O2 +g - l [AFDW] - h- ’ (assuming a figure of 60% ash for this species; Whyte et al., 1987). These values are higher than those reported for other veliger larvae varying from 1.6 to 10 ml 0, *g - ’ *h - I. High values (4.6-15.2 ml 0, *g - ’ *h - ‘) have also been reported for another species of pectinid, A. it-radians(S. Siddall, pers. comm.). Holland & Spencer (1973) reported values of 5-6 ml Oz. g- ’ *h- ’ for 0. edulis larvae based on biochemical changes during starvation, but this technique may produce minimal estimates of energy loss (Bayne, 1983). Whereas respiratory rates appear high in comparison to values for other bivalve larvae, P. ye~~oe~~i~larvae gain enough energy from feeding to exceed the respiratory cost at reasonably low food concen~ations (Fig. 7). The use of well-fed larvae could partially explain the higher metabolic rates observed in this study in contrast to the lower rates obtained for starved larvae in most of the other studies (M. Sprung, pers. comm.). Bivalve larvae migrate vertically at a rate of OS-7 mm - s- ’ and their activity may represent 8-50% of respiratory costs (Zeuthen, 1947; review in Sprung, 1984~). Rates of oxygen consumption are greatly reduced at high larval densities, probably as a result of collisions with other larvae, thereby interrupting swimming and/or feeding activity, or as a consequence of the accumulation of toxic excretory products (Walne, 1966; Millar & Scott, 1967). For example, respiratory rates decrease 35% as the density of P. yefsoensis larvae increases from 5 to 25 * ml - ’ (Fig. 5). Just as high larval density may cause inte~uptions in activity, any physical contact with the surfaces of the respiration chamber may also interfere with swim~ng, feeding or respiratory processes. In order to meaningfully integrate feeding and metabolic studies in bivalve larvae it is necessary to assess their response under realistic conditions, possibly concentrating on the food supply in natural seawater rather than only on artificial diets.
ACKNOWLEDGEMENTS
I would like to thank R. Thompson, S. Siddall, L. Fritz, N. Boume, and C, Hodgson for reviewing the typescript and W. Carosfeld, C. Hodgson, and D. Thompson for technical assistance and helpful discussions in the laboratory. A special thanks to M. Sprung for many helpful suggestions and to J. Whyte for giving me access to some of his unpublished data. While conducting this project at the Pacific Biological Station, Nanaimo, British Columbia, I was supported by a Canadian Government Visiting Postdoctoral Fellowship. New Jersey Agricultural Experiment Station Publication No. D-32001-1-88 supported by state funds. REFERENCES BAYNE,B. L., 1971.Oxygen consumption by three species of lameilibranch molluscs in declining ambient oxygen tension. Camp. Bioehem. Physiol., Vol. @A, pp. 955-970.
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ENERGETICS OF PATINOPECTEN
YESSOENSIS
LARVAE
169
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TENORE,K. R. & W. M. DUNSTAN,1973. Growth comparisons of oysters, mussels and scaHops cultivated on algae grown with artificial medium and treated sewage e&rent. Chesapeake Sci., Vol. 14, pp. 64-66. TETTELBACH,S.T. & E. W. RHODES, 1981. Combined effects of temperature and salinity on embryos and larvae of the northern bay scallop Argopecten irradians irradians. Mar. Biol., Vol. 63, pp. 249-256. THOMPSON,D., N. BOURNE& C. MANSON, 1987. Scallop breeding studies. In, 1983 and 1984 invertebrate management advice, Pacific region, edited by G. S. Jamieson, Can. M.S. Rep. Fish. Aquat. Sci., No. 1848, pp. 97-107. VEN~ILLA,R. F., 1982. The scallop industry in Japan. Adv. Mar. Biol., Vol. 20, pp. 309-382. WALNE, P.R., 1966. Experiments on the large scale culture of the larvae of Ostrea eduZis L. Ftih. Invest. Minist. Agric. Fish. Food. G. Br. Ser. ff Salmon Freshwater Fish., Vol. 25, pp. l-53. WHYTE,J. N. C., 1987. Biochemical composition and energy content of six species of phytoplankton used in mariculture of bivalves. Aquaculture. Vol. 60, pp. 23 1-241. WHYTE, J. N. C., N. BOURNE& C.A. HODGSON, 1987. Assessment of biochemical composition and energy reserves in larvae of the scallop Patinopecten yessoertsis. J. Exp. Mar. Biol. Ecol., Vol. 113, pp. 113-124. Yoo, S. K., 1969. [Food and growth ofcertain important bivalves.] Bull. Pusan F&h. Co&, Vol. 9, pp. 65-87. (In Korean.} ZEUTHEN, E., 1947. Body size and metabolic rate in the animal kingdom with special regard to marine microfauna. C.R. Trav. Lab. Carlsberg Ser. China., Vol. 26, pp. 17-161.