Seasonal partitioning and utilization of energy reserves in two age classes of the bay scallop Argopecten irradians irradians (Lamarck)

J. Exp. Mar. Biol. Ecol., 1988, Vol. 121, pp. 113-136

113

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JEM 01122

Seasonal partitioning and utilization of energy reserves in two age classes of the bay scallop Argopecten irradians h-radians (Lamarck) Jennifer Epp, V. Monica Bricelj and Robert E. Malouf Marine Sciences Research Center, State University of New York at Stony Brook, Stony Brook, New York, U.S.A.

(Received 24 February 1988; revision received 12 May 1988; accepted 25 May 1988) Abstract: Seasonal cycles in body component indices, reproductive condition (determined histologically),

and storage and utilization of protein, lipid and carbohydrate reserves in various tissue pools, were investigated in two cohorts of the bay scallop Argopecten irradians irradians (Lamarck). Scallops were held in cages at two contrasting localities in Long Island, New York, U.S.A. Gametogenesis occurred mainly at the expense of adductor muscle protein and lipid reserves. Energy loss in the adductor muscle could potentially account for 63 to 99% ofthe gonadal buildup in the spring. In contrast to prior studies, digestive gland lipid and muscle carbohydrate made an insignificant contribution to the energy demand during reproduction. In first-year, pre-reproductive scallops, adductor muscle protein also contributed 63-66% of the total energy loss during overwintering stress. Senescence ofolder scallops was evidenced by a more rapid decline in mantle protein reserves than in young individuals. Twenty percent of the older population showed signs of anomalous, advanced oogenesis in March, coincident with the period of highest natural mortality. Results of this study suggest a possible association between senescence and protein metabolism. Contrary to studies showing glycogen to be the main storage product in bivalves such as oysters and mytilids, this study serves to stress the importance of protein as an energy substrate in pectinids. Key words: Argopecten; Biochemical composition; Energy metabolism; Scallop

INTRODUCTION

Many temperate and boreal adult bivalves are capable of storing nutrient reserves in body tissues during periods of high food supply, and subsequently mobilizing them during times of food shortage, decreased rates of feeding, and/or high energy demand (De Zwaan & Zandee, 1972; Ansell, 1974; Comely, 1974; Bayne, 1976; Sastry, 1979; Barber & Blake, 1981; review by Gabbott, 1983). Gametogenesis represents a period of particularly high energy demand, when both maintenance costs and the cost of gamete synthesis must be met by the food supply, stored reserves or a combination of both. The reproductive and biochemical cycles are thus often closely coupled in bivalves and vary Contribution 605 from Marine Sciences Research Center, State University of New York at Stony Brook. Correspondence address: V.M. Bricelj, Marine Sciences Research Center, State University ofNew York at Stony Brook, Stony Brook, NY 11794-5000, U.S.A. 0022-0981/88/$03.50 0 1988 Elsevier Science Publishers B.V. (Biomedical Division)

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both latitudinally and within the same geographic area in relation to the local environment. The bay scallop Argopecten irrudiuns (Lamarck) is a short-lived (<2-yr lifespan) functional hermaphrodite, with a wide distribution along the Atlantic and Gulf coasts of the United States. Populations occurring along its latitudinal range differ considerably in the amplitude and timing of annual spawning events, reproductive output, and the relative importance of specific storage organs (Sastry, 1970; Barber & Blake, 1983; Bricelj et al., 1987a). In mid-latitude, Long Island populations of A. irradians irradians, spawning occurs mainly in June-July, and is followed by rapid somatic growth in the fall, and mass, senescent natural mortality during the winter (Bricelj et al., 1987a,b). The commercial fishery allows for complete removal of post-spawning individuals, since generally few survive to a second spawning. Barber & Blake (1983) suggested that in northern latitudes (Massachusetts), where food availability is higher and temperature-dependent metabolic rates are lower, reproduction in this species is supported through short-term storage in the digestive gland. In southern latitudes (Florida), bay scallop populations exhibit a shift towards utilization of the adductor muscle as the primary storage site. Information about the seasonal partitioning and utilization of biochemical constituents from various tissue pools is only available for A. b-radians concentricus, occurring at the southernmost limit of the species’ distribution (Barber & Blake, 1981). Few studies have investigated age-related changes in energy metabolism in bivalves. Pectinids are ideally suited for such studies because age classes are readily identifiable from external shell growth rings, and gonadal tissue can be easily separated from the visceral mass. Sundet & Vahl(l981) found that immature Chlumys islandica catabolized relatively more of their protein stores than sexually mature scallops during the fall-winter period of nutritive stress. Estabrooks (1973) compared seasonal changes in glycogen and lipid in the digestive gland and gonad of a single cohort of Argopecten irradians irradians over its 2-yr lifespan, but failed to include the adductor muscle, the main storage organ in pectinids, in his study. Relative mortality, and seasonal growth and metabolic rates of first-year (prereproductive) and second-year (post-reproductive) A. irrudiuns irradians from Long Island waters were compared in a preceding paper (Bricelj et al., 1987b). The present study investigates the relative contribution of different tissue pools and biochemical constituents as energy storage sites and substrates in this subspecies, in relation to reproductive and overwintering stress. A further objective of the study is to compare energy utilization of co-existing young and old bay scallop cohorts in an attempt to identify a possible physiological basis for senescence in this species. METHODS

Bay scallops of the 2-yr classes were collected in September 1984 by dredging from Northwest Harbor, eastern Long Island, New York, U.S.A. Scallops were held in cages

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(60 x 60 x 25 cm) at planting densities of 72 first-year and 40 second-year animals per cage, at two locations: Flax Pond, a tidal salt marsh on the north shore of Long Island and Southold, eastern Long Island. Locations and characteristics (temperature, salinity and food availability) of the two sites were described in a previous paper (Bricelj et al., 1987b). Initial shell heights averaged 26.1 and 51.3 mm for young and old cohorts, respectively. Approximately 40 live scallops of each year class were collected at monthly intervals between September 1984 and June-July 1985 from each station. Second-year scallops were only collected through March, since they had all died by the April sampling date, i.e., prior to a second breeding period. Young scallops averaged 50.4 mm by 19 July at Flax Pond, and only 42.8 mm by 12 June at Southold. Older individuals attained 59.1 and 55.7 mm in March at Flax Pond and Southold, respectively. Scallops were held in 0.22~pm filtered seawater at the Flax Pond Marine Laboratory, at ambient temperature and salinity for 48 h prior to any analysis, to allow them to clear their gut contents. The following tissue components were excised from 10 individuals of each year class: adductor muscle, gonad (including the intestinal loop), digestive gland-stomach complex, and remaining tissue (primarily composed of mantle tissue but also including gills, excretory organ, foot, etc.). Dry weight (DW) and ash weight of tissues were determined following oven drying to a constant weight (48 h at 85 “C), and combustion at 450 “C for z 20 h [as recommended by Grove et al. (196 l)]. All weights were determined with an analytical balance to 0.001 mg. The condition index, defined as C.I. = (AFDW of component tissue/AFDW of total tissue) x 100, was determined for each tissue pool. Total DW of tissues was computed from the sum of the different tissue components for these 10 animals, plus the total tissue DW of ten additional scallops used to determine metabolic rates by Bricelj et al. (1987b). Fewer individuals were available for DW from Southold (Table II). Another 10 scallops were dissected into tissue components and like tissues were pooled within each year class and lyophilized overnight. They were subsequently pulverized using a mortar and pestle, and lyophilized for an additional 12 h. These tissues, used for proximate analysis, were stored in air-tight vials, in turn stored with desiccant at - 20 “C. Freeze-dried tissues were used, since Ivell (1983) showed that oven-drying can cause a 20-25% underestimate of the energy content of mollusc tissues due to the volatilization of lipids. Mean condition indices of the two cohorts were compared using a two-tailed t test of difference between means (Sokal & Rohlf, 1981). Transformation of data was not required since normality of condition indices was ascertained for a fairly large sample (n = 49) of first-year scallops collected in December (Kolmogorov-Smirnov test for goodness of fit). Homogeneity of variances was tested using Hartley’s F,,, test (Sokal & Rohlf, 1981). Protein content of two to five replicate samples was determined by CHN analysis using atropine as standard. A conversion factor of 5.8 was used to obtain protein from nitrogen values (Gnaiger & Bitterlich, 1984). These investigators found that proximate composition determined from stoichiometric CHN analysis and direct biochemical

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analysis agreed within 10%. The coefficient of variation [C.V. = (SD/$ x 1001 in protein content among replicates averaged 2.6%. Total carbohydrate was determined in triplicate using a calorimetric phenol-sulphuric acid method (Gerhardt, 1981). Absorbance at 440 nm was measured with a Bausch & Lomb 70 spectrophotometer, and compared to a glucose standard. The C.V. among replicates averaged 4.4%. Total lipid was determined gravimetrically (in triplicate), following extraction in 2 : 1 chloroform-methanol using z 50 mg of tissue (Bligh & Dyer, 1959). Extracted lipids were evaporated to dryness on aluminum foil pans under a nitrogen stream, and weighed to 0.001 mg with a Cahn electrobalance. The C.V. among replicates averaged 6.5 %. All samples were corrected for differences between lyophilized and oven-dried weight in order to express composition on a dry weight basis. Results of the biochemical analysis are expressed in mg (absolute value) per standardsized scallop following methods used by Ansell (1974), Ansell & Trevallion (1967) and Robinson et al. (198 1). To calculate the biochemical composition of a standard scallop, geometric mean (GM) regressions of log total tissue DW on log shell height were calculated for each year class at each sampling date. Functional regressions were used since GM parameters are less sensitive to variation in the size range of animals used (Ricker, 1973). The shell height of a standard animal was chosen as the mean of all shell heights measured for a cohort at a site over the entire experimental period. Use of this method has been recently called into question by Hilbish (1986) and Borrero & Hilbish (1988) under conditions in which shell and tissue growth patterns are uncoupled. In the present study negligible shell growth occurred during most of the experimental period. Older scallops experienced negligible shell growth after the October sampling date, while shell growth of young scallops ceased in November-December (Bricelj et al., 1987b). The amount of a biochemical constituent (e.g., mg protein) in each tissue component of a standard animal was thus calculated as follows: DW of biochemical constituent = body component DW of standard scallop x biochemical content (% DW). The body component DW was determined from the product of the total tissue DW of a standard animal, predicted from GM regressions, and the mean tissue condition index (expressed on a DW basis). Since biochemical composition was determined from pooled tissue samples, confidence limits could not be estimated from the resulting values. Energy conversion factors for carbohydrate and lipid (chloroform-methanol extraction)were4.10and8.42 kca.l*g-‘(17.2and35.3 kJ.g-‘;Brody, 1945;Beukema & De Bruin, 1979, respectively). An energy conversion factor of 4.8 kcal *g - i protein (20.1 kJ *g- ‘) was adopted in this study to account for incomplete protein oxidation in ammonotelic animals (Kersting, 1972), as suggested by Beukema & De Bruin (1979). The remaining 10 scallops of each monthly collection were used for histological examination of the gonad, following standard methods (Humason, 1979). Gonads were preserved in Bouin’s fixative. A transverse section including both male and female portions of the gonad was embedded in Paraplast, sectioned to 5-pm thickness and stained with hematoxylin and eosin. Gametogenic state was characterized based on the stages described by Sastry (1963, 1966) and Taylor & Capuzzo (1983), and only

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reported for the ovarian section of the hermaphroditic gonad. Mean oocyte diameter was determined from histological sections by measuring the maximum diameters of 20 oocytes from each of 10 scallops using a compound microscope with a graduated eyepiece. The mean number of residual oocytes per follicle of post-spawning secondyear scallops was obtained by examining 30 follicles in each scallop in which ripe oocytes were apparent.

RESULTS

CONDITION

INDICES

Rapid growth of Flax Pond scallops during the fall was reflected in an 1l- and 1.6-fold increase in mean adductor muscle weight between September and January for first- and second-year individuals, respectively (Appendix I). Fig. 1 shows fluctuations in mean body component condition indices for the two age classes at Flax Pond. The adductor muscle C.I. of young scallops increased by 27.2% from September to October, remained relatively constant from October to April, and declined sharply, by 42.9 %, from April to June. The inverse relationship between the gonadal and muscle condition indices during the spring indicates that gametogenesis and gonadal buildup take place at the expense of adductor muscle reserves. The mean adductor muscle C.I. of second-year scallops remained relatively constant and was greater than that of first-year scallops. This difference was statistically significant only during the early part of the experiment (Table I). The gonadal C. I. of first-year scallops showed little change from September to April, then increased rapidly, from 6.0 to a maximum of 29.2% in June. The decline in gonadal C.I. during June-July reflects spawning activity. The gonadal C.I. of second-year scallops experienced little change throughout the experimental period. The “other” tissues C. I. declined from September to October for first-year scallops, remained constant throughout the winter, and declined by 18.1 y0 from April to May, suggesting that this tissue pool may play a secondary role in contributing reserves during gonadal buildup. The C. I. of “other” tissues for second-year scallops remained constant and was significantly different (lower) than that of young scallops throughout the period when the two cohorts co-occurred (Table I). The digestive gland C.I. showed no seasonal variation and exhibited comparable values in both cohorts. This tissue pool thus appeared to play a negligible role in the transfer of stored reserves to the developing gonad, in contrast to findings reported for bay scallop populations in Massachusetts (Sastry, 1970). Seasonal changes in condition showed similar patterns at the two sites (Figs. l-2). At Southold the adductor muscle and “other” tissue condition indices both declined (by 41.2 and 25.9%) respectively) during the period of gametogenesis. At this site the gonadal C.I. attained a maximum of 32.0% a month earlier than at Flax Pond, reflecting

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the earlier spring warming of waters at Southold, the shallower site. There was no significant dflerence (P 2 0.1) between the maximum gonadal C. I. of first-year scallops at Flax Pond (mean k SD = 29.2 + 5.96, n = 20) and Southold (32.1 f 3.08, n = 10). Thus, although individuals held at Southold experienced more stressful environmental TABLE

Comparison

of mean

Month Flax Pond Adductor muscle S 0 N J

F M “Other” tissues S 0 N J F M Southold Adductor muscle 0 D J F M “Other” tissues 0 D J F M a NS = not significant,

I

condition indices (calculated on an AFDW basis; standard between brackets) of scallop tissues (see Methods). lst-yr

2nd-yr

36.42(2.78) 46.31(3.04) 42.91(3.80) 44.54(3.61) 44.30(2.46) 46.15(3.73)

50.81(3.90) 48.68(2.80) 49.19(5.31) 46.87(2.94) 46.12(3.39) 48.02(3.74)

41.56(2.02) 34.68(2.49) 35.21(3.26) 33.46(2.75) 34.49( 1.75) 33.97(2.51)

30.34(3.01) 29.93( 1.60) 30.77(3.83) 31.13(1.81) 31.65(1.89) 3 1.37(2.43)

40.41(2.78) 40.83(3.57) 39.87(2.31) 37.07(2.26) 41.45(4.00)

46.50(3.51) 41.20(4.74) 44.44(5.38) 43.24(3.51) 45.61(3.04)

36.10(2.41) 37.07(2.90) 37.96(2.26) 39.65(1.74) 36.98( 1.96)

31.87(3.15) 33.50(2.08) 33.20(3.50) 35.85(1.72) 34.82(2.13)

P > 0.05; *0.05 > P> 0.01; **0.01 > P> 0.001; ***p<

deviation

indicated

Significance”

*** NS ** NS NS NS

*** *** * * ** *

*** NS * *** *

*** ** ** *** * 0.001

conditions, and attained a lower maximum shell height (Bricelj et al., 1987b), both populations devoted a comparable fraction of their body mass to reproduction. As observed at Flax Pond, the mantle C.I. was significantly lower for second-year scallops than for first-year individuals, while the muscle index was greater in the older cohort (Table I). Older scallops at both stations showed no significant decline in C.I.‘s of any tissue pool during the period of mass senescent natural mortality, which occurred between December and March (Bricelj et al., 1987b).

UTILIZATION

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OTHER

I

I

I

TISSUES

FLAX

POND

DIGESTIVE

DIGESTIVE

0

119

!

!

!

ADDUCTOR

I

!

I

i

’

MUSCLE

GONAD GONAD

IO-

0

**

1

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h

S’O’N’D’J’F’M’A’M’J’J

*.

a

Is1 year

J

8

c

cohort

c

-

I

m

2nd

I&

S

1

O’N’D’J’F’M’A’M’J’J

MONTHS

Fig. 1. Mean body component confidence intervals for Flax

5

ADDUCTOR

cohort ”

MONTHS

condition indices (calculated on an ash-free dry weight basis) and 95% Pond first-year (open symbols) and second-year bay scallops (closed symbols).

I

DIGESTIVE

50 -

year

2

”

OTHER

SOUTHOLD

TISSUES

DIGESTIVE

MUSCLE

30-

t= $

20-

z

GONAD

T

IO -

d ’

1st year

cohort

GONAD

e

2nd yeor

cohort

S’O’N’D’J’F’M’A’M’J’J’S’O’N’D’J’F’M’A’M’J’J MONTHS

Fig. 2. Body component

MONTHS

condition indices (mean and 95% confidence intervals) symbols) and second-year scallops (closed symbols).

for Southold

first- (open

-I

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BIOCHEMICAL

COMPOSITION

Fig. 3 shows the biochemical composition (mg of each biochemical constituent) of standard sized first-year scallops at the two study sites. The proximate composition of each tissue pool (as a yO of dry weight), used to construct this figure, is shown in FLAX

POND

- 1st year

cohort

SOUTHOLD

- 1st year

cohort

I50

Protein A Carbohydrate 9 Lipid

/

l

100

ADDUCTOR

-&

E -

MUSCLE

ADDUCTOR MUSCLE

150

t.:’

;OLT’1’;-, SbNDJFMAMJ

MONTHS

“OTHER”

MONTHS Fig. 3. Biochemical composition (mg of protein, lipid and carbohydrate) of a standard-sized first-year scallop (45 mm in shell height) at Flax Pond, and at Southold (40 mm standard size).

Appendices I and II. The sum of the biochemical components is often somewhat greater than the total dry weight, probably reflecting cumulative errors in the various analytical methods employed. Such excessive or incomplete mass recoveries are typically found in studies involving direct biochemical determinations. Parameters of geometric mean

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regressions used in calculating the total tissue DW of a standard-sized scallop (see Methods) are provided in Table II. In both cohorts, protein was the main constituent of all tissues, especially in the adductor muscle where protein contributed up to 74-76% of the dry weight. At Flax Pond, all biochemical constituents in the muscle of first-year scallops increased during TABLE II

Geometric

mean regression parameters of total dry tissue weight (W, in mg) on shell height (H, in mm) following the relationship: log W = a + 6 log H (r2 = coefftcient of determination).

Flax Pond Date

a Y intercept

b slope

r2

n

- 2.0843 - 3.8363 - 3.0357 - 2.4006 - 2.1668 - 2.3604 - 2.1266 - 3.8424 - 1.6653 - 2.4992

2.1564 4.1561 3.6070 3.2335 3.0927 3.2080 3.0414 4.1200 2.8048 3.2791

0.859 0.848 0.698 0.865 0.659 0.800 0.596 0.561 0.627 0.484

38 20 22 18 21 25 21 22 31 23

-

2.8630 3.9149 2.5273 2.7964 3.8490 2.4735

0.740 0.329* 0.669 0.301* 0.663 0.507

17 19 20 16 21 21

a

b

r*

n

- 3.1676 - 2.8419 - 1.7936 - 3.1066 -4.0101 - 3.8217 - 2.2582 - 2.2578

3.6978 3.5197 2.8763 3.6745 4.2504 4.0950 3.1689 3.1851

0.860 0.871 0.866 0.938 0.871 0.742 0.696 0.479*

10 9 23 9 10 11 10 10

Oct.

- 3.7866

Dec. Jan. Feb. Mar.

-

4.0548 4.0336 3.1223 3.0873 3.2110

0.721 0.623 0.563 0.881 0.685

20 10 14 10 14

First-year scallops Sep.

Oct. Nov. Jan. Feb. Mar. Apr. May Jun. Jul. Second-year scallops Sep. Oct. Nov. Jan. Feb. Mar.

1.7188 3.5304 1.0571 1.5583 3.4502 1.0333

Southold Date First-year scallops

Oct. Dec. Jan. Feb. Mar. Apr. May Jun. Second-year scallops

* Correlation

coefficient

3.7221 2.1298 2.0829 2.3718

r is significant

at P < 0.05; in all other cases it is significant

at P i 0.01.

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September-October, and declined during October-November. During the latter period of negative energy balance, protein in the muscle of a standard animal declined by 28 y0 and was the principal adductor muscle reserve used to meet metabolic demands in young scallops. The loss of muscle protein amounted to 63% of the total caloric loss (protein + lipid + carbohydrate) occurring in this tissue (Table III). Size-normalized TABLE III

Percent

contribution

(A) During

of protein,

late fall-winter

lipid, and carbohydrate to the total caloric loss in the adductor a standard first-year scallop.

muscle of

starvation % Contribution

Substratum

a Calculated b Calculated (B) During

Protein Lipid Carbohydrate October through November December through February

Flax Pond” 62.6 18.7 18.6

gametogenesis (March-June) Substratum

Flax Pond

Protein Lipid Carbohydrate

49.6 43.4 7.0

Southoldb 66.5 20.5 13.0

Southold 38.0 56.1 5.9

adductor muscle protein and lipid declined again, by 36 and 77 %, respectively, during gametogenesis in the spring. The percent contribution of protein, lipid, and carbohydrate to the total caloric loss in the adductor muscle during gametogenesis is indicated in Table III. During the reproductive period, 99% of the caloric gonadal buildup could be accounted for by the energy loss of the adductor muscle, illustrating its major role in fueling reproduction. Direct transfer of nutrients between these organs, however, can only be conclusively demonstrated using labelled substrates. The protein level of the adductor muscle of second-year Flax Pond scallops increased during the fall, and declined by 23.0% during the winter (November-February; Fig. 4). Muscle protein, lipid and carbohydrate contributed 56.3, 20.0 and 23.6% respectively to the total energy loss in this tissue. This decline was followed by a marked, unexplained increase in protein during February-March, which is caused both by an increase in the % protein content (from 64 to 742, Appendix I) and an increase in the standardized dry weight (from 840 to 883 mg) of the muscle. Gonadal tissue reserves remained relatively constant in pre-reproductive Flax Pond scallops until the spring, when gametogenesis was associated with a major buildup in gonadal protein, and a less pronounced increase in gonadal lipid and carbohydrate levels. The “other” tissues of first-year Flax Pond scallops showed a gradual decline

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in reserves, especially protein, between October and July. In contrast, protein levels of “other” tissues in older scallops decreased sharply from January to February, during the period when the highest mortality rate was recorded (Bricelj et al., 1987b). Protein contributed 88.8% to the total mantle energy loss (protein + lipid + carbohydrate) in this age class. The digestive gland did not appear to play a role as a storage organ in either cohort. FLAX

POND

100

50

100

E

!k---c DIGESTIVE

600

c

500 -

400 -I

“OTHER”

ADDUCTOR MUSCLE

300

I:‘[\

IOC

i

I

S

ONDJ

I

I

1

I

FM

z ‘r

I I SONDJFM

_ I

I

I

1

MONTHS Fig. 4. Biochemical composition (in mg) of a standard-sized second-year scallop (57 mm in shell height) at Flax Pond (symbols as in Fig. 3).

In many respects, first-year scallops showed similar patterns of energy utilization at the two sites (Fig. 3). At Southold, however, the adductor muscle showed less of a buildup of reserves during the fall. Muscle protein dropped by 17.4% between December and February, and declined by a further 25 y0 during gonadal development in the spring. The “other” tissues at Southold did not show a decline in protein during the late fall-winter months as observed at Flax Pond, but exhibited a more pronounced decline in reserves during gametogenesis. At this site energy loss in the adductor muscle and mantle tissues could account for 62.9 and 49.6%, respectively, of the spring gonad buildup.

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Second-year scallops at Southold (Fig. 5) showed similarities in the pattern of energy utilization, particularly of the gonad and mantle, when compared to the same cohort at Flax Pond. The adductor muscle protein declined by 15% from October to early December. As at Flax Pond, the muscle protein content increased from 75 to 84%,

450

400

350

300

,50

ADDUCTOR

MUSCLE

P

150 F

t

look- , SONDJFM

“OTHER”

I

I

1

I

I

SONDJFM

MONTHS Fig. 5. Biochemical

composition

(in mg) of a standard-sized second-year Southold (symbols as in Fig. 3).

scallop (55 mm in shell height) at

between February and March (Appendix II). At both stations mantle protein declined considerably (by 25 and 2 1y0 at Flax Pond and Southold, respectively) during the winter period of mass mortality. Gonad lipid content (as a y0 of DW) was on the average two to three times higher in immature scallops than in post-reproductive individuals at both study sites (Appendices I, II). REPRODUCTIVE

DEVELOPMENT

Table IV gives mean oocyte diameters, indicative of the stage of reproductive development, for scallops at the two sites. In September, pre-reproductive scallops (3-4 months old) were immature, while second-year scallops (13-14 months old) were in a “spent” condition. Gonadal follicles were mostly empty, with some follicles containing few ( < 2) residual ripe oocytes (Table V). Scallops of both age classes remained in a reproductive “resting” stage until March. Both cohorts showed early signs of gametogenesis in March, with some cells undergoing cytoplasmic growth. At this time, no differences were observed between most first- and

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second-year scallops. Two out of 10 older scallops at each station, however, exhibited anomalous, advanced reproductive development in March. Ripe, intact and degenerating, resorbing oocytes, surrounded and invaded by phagocytic cells, occurred in these individuals (Fig. 6). Numerous such phagocytic cells were present in the connective tissue between follicles as well as in the lumen of the follicles. These ripe oocytes did not appear to be residuals from the previous spawning season, since residuals were totally absent from follicles of second-year individuals in the early winter months (November to February), and the number of ripe oocytes per follicle in these anomalous individuals was considerably greater in March than during the fall (Table V). In agreement with information provided by the gonad condition index, histological analysis showed that scallops were fully ripe, with densely packed ovarian follicles, by 19 May at Southold, and a month later, by 21 June, at Flax Pond. TABLE IV

Mean oocyte diameter (pm) determined from histological sections of scallop gonads. Month

Jan. Feb. Mar. Apr. May Jun. Jul.

Year class

Oocyte diameter

First Second First Second First Second First First First First

(SE)

Flax Pond

Southold

2 (0.57) 1 (0.22) 4 (0.33) 3 (0.20) 14 (3.00) 19 (4.80) 25 (6.39) 39 (3.83) 55 (2.97) 37 (4.24)

1 (0.06) 1 (0.13) 3 (0.32) 3 (0.23) 12 (3.38) 18 (6.51) 30 (6.39) 40 (5.00) 56 (10.15)

TABLE V

Incidence and number of ripe oocytes present in second-year scallops, fall 1984-winter 1985. Date (A) Flax Pond Sep. Oct. Nov. Jan. Feb. Mar. (B) Southold Oct. Dec. Jan. Feb. Mar.

% of scallops with ripe oocytes

Mean no. of ripe oocytes per follicle

40 60 0 0 0 20

1.0 0.5 0 0 0 5.0

30 20 0 0 20

2.0 0.2 0 0 6.0

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Fig. 6. Microphotographs of female gonadal histological sections of bay scallops in March 1985. Upper 1~:ft: first-year scallop; lower left: second-year scallop representative of 80% of the sampled population; upI )er and lower: second-year scallop representative of 20% of the sampled population, showing anomalc MS presence of ripe oocytes (see text for explanation).

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DISCUSSION ENERGY

METABOLISM

DURING

GAMETOGENESIS

Sastry (1970) found an inverse relationship between the digestive gland and gonadal condition indices of bay scallop populations from Nantucket Sound, Massachusetts, suggesting that transfer of energy reserves occurred between these tissue pools during reproduction. In contrast, no relationship was found between the digestive and gonadal indices in a Florida population of the southern bay scallop A. it-radiansconcentricus, and the adductor muscle was identified as the primary site of reproductive energy storage in this subspecies (Barber & Blake, 1983). In the present study, analysis of condition indices of a mid-latitudinal scallop population at two differing sites, showed that reproduction occurred largely at the expense of adductor muscle reserves. Previous studies have emphasized the importance of the adductor muscle as an energy storage site in pectinids (Ansell, 1974; Taylor & Venn, 1979), and related it to the scallop’s need for a readily available source of energy for locomotion. In this study, no change in digestive gland condition index was associated with reproduction, suggesting that this tissue did not serve as a storage site, although it is known to play an important role in regulating the distribution of assimilated nutrients to body tissues (Sastry & Blake, 1971; Vassallo, 1973). A decline in the condition of “other” tissues occurred during gonadal buildup however, suggesting that the mantle may play a role of secondary importance as an energy storage site. A decline in the “other” tissues index during gonad growth was also observed in bay scallop populations from North Carolina and Nantucket Sound (Sastry, 1979). Biochemical analysis provides a more thorough understanding of seasonal energy storage and utilization cycles in bivalves. In a study of the southern bay scallop A. irradians concentricus, gonad development took place primarily at the expense of adductor muscle protein, and to a lesser extent at the expense of muscle glycogen and digestive gland lipid (Barber & Blake, 1981). A decline in digestive gland lipid stores in conjunction with gametogenesis has also been described in the northern scallop, A.i. irradians (Estabrooks, 1973) and in Placopecten magellanicus (Robinson et al., 1981). No depletion of digestive gland reserves was observed in the present study. In this study, 63 to 99% of the total energy gain by the gonad could be potentially explained by coincident loss of energy reserves from the adductor muscle. At both study sites this loss was mainly attributed to protein and lipid decline. Muscle reserves are, however, not entirely adequate to sustain energy demands during gonad growth. Sastry (1966, 1979) found that storage material alone was insufficient to complete gonadal maturation in Argopecten from North Carolina, and that an exogenous food supply was also necessary. Although in the present study mantle protein reserves also declined during gonadal development, especially at Southold, the high metabolic demand during spring reproduction (estimated by Bricelj et al., 198713)must therefore be at least partially met by the external nutrient supply. Carbohydrate reserves in the adductor

UTILIZATION

OF SCALLOP’S

ENERGY

RESERVES

129

muscle made a negligible contribution to the energy demand during gonadal development. This finding differs from results of previous studies with this (Barber & Blake, 198 1) and other pectinid species such as Pecten maximus (Comely, 1974) and Chlamys opercularik (Taylor & Venn, 1979) in which energy demands during gametogenesis were supported by both adductor muscle protein and glycogen, rather than protein and lipid. For example, Barber & Blake (1985) estimated that adductor muscle protein contributed 11773 J of energy compared to 4805 J provided by muscle glycogen during gametogenesis. In our study the contribution of the external food supply to the total energy demand was probably sufficient to allow conservation of adductor muscle glycogen for anaerobic energy production. The latter is required to sustain muscle activity during swimming and predator avoidance in pectinids (De Zwaan et al., 1980). Our study emphasizes the important role of somatic protein and lipid reserves in supporting energy demands during reproduction in scallops. This contrasts with the preferential use of carbohydrate (glycogen) as an energy reserve, particularly during early gametogenesis, in Mytilus edulis (Gabbott, 1975). Traditional focus on the importance of glycogen in bivalve energy metabolism (especially of mussels and oysters), has led to omission of protein in studies of biochemical cycles of pectinids (e.g., Estabrooks, 1973; Robinson et al., 198 1). The enhanced ability of Mytilus edzdis to store glycogen has been related to the presence of well-developed vesicular and adipogranular glycogen storing cells in mantle connective tissue of this species (Lubet, 1959; Bayne et al., 1982). This storage capability is reflected in a typically high seasonal maximum glycogen content of 42 to 53% in the mantle of M. edulis (De Zwaan & Zandee, 1972; Gabbott, 1983). In contrast, the carbohydrate content of the adductor muscle, the main site for storage of reserves in pectinids, attained a maximum of only 23.5-25.5% in first-year scallops (Appendices I, II). Throughout the study period the adductor muscle carbohydrate content was about 27 to 37% higher in second-year than in first-year scallops. This agrees with Sundet & Vahl’s (1981) observation that the glycogen content of the muscle was higher in sexually mature than in immature Chlamys islandica. ENERGY

METABOLISM

DURING

OVERWINTERING

In young scallops, energy utilization during the winter was reflected in protein loss, mainly from the adductor muscle. These results are comparable to those described for Tapesphilippinarum, in which somatic protein contributed a dominant fraction (74%) of the maintenance energy during the winter (Beninger & Lucas, 1984). The use of protein to meet metabolic demands during periods of prolonged nutritive stress has been extensively documented, under both field and laboratory conditions, in European populations of M. edulis (Gabbott & Bayne, 1973; Bayne, 1976; Pieters et al., 1979; Bayne et al., 1982). In mussels, however, protein utilization only occurs after glycogen stores have been relatively depleted. Second-year scallops also evidenced a marked decline in protein reserves, both from the adductor muscle and mantle, during the winter. Energy storage and utilization

J. EPP ETAL.

130

patterns however, are not as clear to interpret in older as in young individuals. At Flax Pond, senescent scallops experienced a more accelerated decline in mantle protein than young individuals. Although both cohorts lost 25% of their mantle protein, in older scallops this loss occurred during the month of January at a rate of 0.75 y0 . day- ‘, while in young scallops it took place gradually over a 3-month period (0.35% * day- ’ between 22 October and 3 February). At Southold, mantle protein loss during the winter was only experienced by the older cohort. It is interesting to point out that this decline coincided with the period of highest mortality rates (Bricelj et al., 1987b). Older scallops also showed greater fluctuations in muscle protein levels during the winter. Results of net protein balance in total somatic tissues (mantle + adductor muscle + digestive) reveal than young and old scallops experienced similar relative protein losses during overwintering (23 y0 for first-year, and 19% for second-year scallops at Flax Pond). This differs from Sundet & Vahl’s (198 1) results for the longer lived Chlamys islandica. In this species, in agreement with theoretical expectations, mature scallops (shell height = 50-55 mm, age = 5-8 yr) catabolized relatively less of their body protein (16%) than immature scallops (56% ; 20-30 mm, age = 2-4 yr). Results of the present study thus suggest that future work should examine in more detail the relationship between protein metabolism (whole body rates of protein synthesis and breakdown) and senescence. Such studies should incorporate examination of individual variability, since there is evidence of considerable variability in the timing of death (Bricelj et al., 1987b), and in reproductive condition (this study) within a second-year cohort. Ansell & Sivadas (1973) postulated that increased loss of protein might increase the likelihood of mortality in natural and experimental populations of the bivalve Donax vittatus.Tait (1986) showed that in another semelparous mollusc, Octopus vulgaris, senescent individuals exhibited higher rates of in vitro net breakdown of protein in the mantle musculature than either pre-reproductive fed or starved individuals. He attributed post-reproductive death in this species to the action of optic gland hormones on protein metabolism. It is important to note that results of this study were obtained for animals disturbed by transplanting to two new habitats, and thus must be extrapolated with caution to natural populations. The high early survival and growth rates of scallops at the Flax Pond site (Bricelj et al., 1987b) do suggest, however, that these individuals were not unduly stressed by our manipulations. Parallel sampling of the two cohorts from wild populations cannot be achieved in this region, where second-year scallops are heavily exploited following opening of the harvesting season in September.

REPRODUCTIVE

DEVELOPMENT

Mean egg sizes at the peak of the reproductive period were similar (55-56 pm) at the two stations. Oocyte size, as determined histologically in this study, was comparable to the size of unfertilized oocytes (54 pm) spawned by Long Island scallops, as determined with a Coulter Counter by Bricelj et al. (1987a). Barber & Blake (1983) suggested

UTILIZATION

OF SCALLOP’S

ENERGY

RESERVES

131

that in Argopecten irradians, maximum oocyte size decreases with decreasing latitude along the east coast of the U.S.A. This latitudinal pattern is not entirely substantiated when data from the present study are included (Fig. 7). Maximum oocyte size of Long Island scallops (55 pm; latitude 41 ON) was smaller than that of North Carolina scallops 90

80

0

l

Woods

0

Flax

Hole,

A

Beaufort.

MA

Pond,NY NC’

J’F’M’A’M’J’J’A’S’O’N’D’ MONTHS

Fig. 7. Changes in mean oocyte diameter of east coast populations of Argopecfen iwadians during the reproductive cycle [New York, first-year scallops, present study; Massachusetts and North Carolina scallops, Sastry (1970); Florida scallops, Barber & Blake (198311. Bracketed numbers indicate stages of the gametogenic cycle: (1) immature; (2) resting; (3) oogonia and cytoplasmic primary growth; (4) cytoplasmic growth and vitellogenesis; (5) vitellogenesis and maturation; (6) ripe; (7) spawning.

(68 pm, Sastry 1970; latitude 35”N). As discussed by Bricelj et al. (1987a) the small oocyte size (3 1 pm) of Florida scallops may be due to more protracted spawning and greater asynchrony in development in southern populations. Indeed, Barber & Blake (198 1) reported a maximum pre-spawning oocyte diameter exceeding 50 pm in Florida scallops. There remains, however, a large unexplained difference in oocyte size between Massachusetts (90 pm) and New York (55 pm) scallop populations, although both exhibit a relatively discrete spawning period (Fig. 7). Histological examination of the gonads revealed that first-year and most second-year scallops experienced synchronous reproductive development. Anomalous, premature development with oocyte lysis and resorption was observed, however, in 20% of the

132

J. EPP ETAL.

older cohort in March. Since it has been established that the gametogenic cycle is closely linked with the neurosecretory cycle in bivalves (Lubet, 1959; Blake & Sastry, 1979), this might suggest a neuroendocrine disturbance in senescent individuals. The relationship between neurosecretory activity, protein metabolism and senescence in this species warrants further investigation.

ACKNOWLEDGEMENTS

This work was sponsored by N.O.A.A. National Sea Grant College Program Ofice, Department of Commerce, under grant number NA86AA-D-SG045 to the New York Sea Grant Institute. We thank W. Smith and C. McCarthy from the Suffolk County Community College, Long Island, New York, for their cooperation, and R. Castaneda for help in field sampling.

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scallops Argopecten irradiuns irrudians (Larnarck): mortality, growth, and oxygen consumption. J. Exp. Mar. Biol. Ecol., Vol. 110, pp. 73-91. BRODY, S., 1945. Bioenergetics and growth. Reinhold, New York, New York, 1023 pp. COMELY,C. A., 1974. Seasonal variations in weights and biochemical content of the scallop Pecten maximus L. in the Clyde Sea area. J. Cons. Cons. Int. Explor. Mer., Vol. 35, pp. 281-285. ESTABROOKS,S. L., 1973. Seasonal variation in the glycogen and lipid content of the bay scallop, Argopecten irrudiuns Lamarck. M. S. thesis, Northeastern University, Boston, Massachusetts, 68 pp. GABBOTT,P.A., 1975. Storage cycles in marine bivalve molluscs: a hypothesis concerning the relationship between glycogen metabolism and gametogenesis. In, Proc. Ninth Eur. Mar. Biol. Symp., edited by H. Barnes, Aberdeen University Press, Aberdeen, U.K., pp. 191-211. GABBO-~T,P. A., 1983. Developmental and seasonal metabolic activities in marine molluscs. In, The Mollusca. Vol. 2. Environmental biochemistry andphysiology, edited by P.W. Hochachka, Academic Press, New York, New York, pp. 165-217. GABBOTT,P. A. & B. L. BAYNE, 1973. Biochemical effects of temperature and nutritive stress on Mytilus edulis L. J. Mar. Biol. Assoc. U.K., Vol. 53, pp. 269-286. GERHARDT,P., 1981. Manual of methodsfor general bacteriology. Am. Sot. Microbial., Washington, District of Columbia, pp. 332-334. GNAIGER,E. & G. BIT~ERLICH,1984. Proximate biochemical composition and caloric content calculated from elemental CHN analysis: a stoichiometric concept. Oecologiu (Berlin), Vol. 62, pp. 289-298. GROVE,E. L., R. A. JONES & W. MATHEWS,1961. The loss of sodium and potassium during the dry ashing of animal tissue. Analyt. Biochem., Vol. 2, pp. 221-230. HILBISH,T. J., 1986. Growth trajectories of shell and soft tissue in bivalves: seasonal variation in Mytilus edulis L. J. Exp. Mar. Biol. Ecol., Vol. 96, pp. 103-l 13. HUMASON,G. L., 1979. Animal tissue techniques. W. H. Freeman & Co., San Francisco, California, fourth edition, 661 pp. IVELL,R., 1983. Technical note: the preparation of molluscan tissue for production estimates. J. MON.Stud., Vol. 49, pp. 18-20. KERSTING,K., 1972. A nitrogen correction for caloric values. Limnol. Oceanogr., Vol. 17, pp. 643-644. LUBET,P., 1959. Recherches sur le cycle sexuel et f&mission des gametes chez les Mytilides et les Pectinides. Rev. Trav. Inst. Peches Mat-it., Vol. 23, pp. 389-548. PIETERS, H., J. H. KLUYTMANS,W. ZURBURG& D. I. ZANDEE, 1979. The influence of seasonal changes on energy metabolism in Mytilus edultk (L.). 1. Growth rate and biochemical composition in relation to environmental parameters and spawning. In, Cyclicphenomena in marineplants and animals, edited by E. Nayor & R.G. Hartnoll, Pergamon Press, Oxford, U.K., pp. 285-292. RICKER,W. E., 1973. Linear regressions in fishery research. J. Fish. Res. Board Can., Vol. 30, pp. 409-434. ROBINSON,W. E., W. E. WEHLING,M. P. MORSE & G. C. MCLEOD, 1981. Seasonal changes in soft-body component indices and energy reserves in the Atlantic deep-sea scallop, Placopecten magellunicus. Fish. Bull. NOAA, Vol. 79, pp. 449-458. SASTRY,A.N., 1963. Reproduction of the bay scallop, Argopecten irradians Lamarck. Infuence of temperature on maturation and spawning. Biol. Bull. (Woods Hole, Mass.), Vol. 125, pp. 146-153. SASTRY,A.N., 1966. Temperature effects in reproduction of the bay scallop, Argopecten irradians Lamarck. Biol. Bull. (Woods Hole, Muss.), Vol. 130, pp. 118-134. SASTRY,A. N., 1970. Reproductive physiological variation in latitudinally separated populations of the bay scallop, Argopecten irradians Lamarck. Biol. Bull. (Woods Hole, Mass.), Vol. 138, pp. 56-65. SASTRY,A. N., 1979. Pelecypoda (excluding Ostreidae). In, Reproduction of marine invertebrates, edited by A. C. Giese & J. S. Pearse, Academic Press, New York, New York, pp. 113-283. SASTRY,A. N. & N. J. BLAKE,1971. Regulation ofgonad development in the bay scallop Argopecten irradians Lamarck. Biol. Bull. (Woods Hole, Mass.), Vol. 140, pp. 274-283. SOKAL, R.R. & F.J. ROHLF, 1981. Biometry. W.H. Freeman & Co., San Francisco, California, second edition, 859 pp. SUNDET,J. H. & 0. VAHL, 1981. Seasonal changes in dry weight and biochemical composition of the tissues of sexually mature and immature Iceland scallops, Chlamys islundica. J. Mar. Biol. Assoc. (I. K., Vol. 6 1, pp. 1001-1010. TAIT, R. W., 1986. Aspects de la senescence post reproductive chez Octopus vulgaris. Doctoral dissertation, Universite Paris VI, France, 250 pp. TAYLOR,A. C. & T. J. VENN, 1979. Seasonal variation in weight and biochemical composition of the tissues

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of the queen scallop, Chlamys opercularis, from the Clyde Sea area. J. Mar. Biol. Assoc. U.K., Vol. 59, pp. 605-621. TAYLOR,R.E. & J.M. CAPUZZO, 1983. The reproductive cycle of the bay scallop, Argopecten irradians irradians (Lamarck), in a small coastal embayment on Cape Cod, Massachusetts. Estuaries, Vol. 6, pp. 431-435. VASSALLO,M.T., 1973. Lipid storage and transfer in the scallop Chlamys hericia Gould. Comp. Biochem. Physiol., Vol. 44A, pp. 1169-l 175. DE ZWAAN, A. & D. I. ZANDEE, 1972. Body distribution and seasonal changes in the glycogen content of the common sea mussel Mytilus edulis. Comp. Biochem. Physiol., Vol. 43A, pp. 53-58. DE ZWAAN, A., R. J. THOMPSON& D. R. LIVINGSTONE,1980. Physiological and biochemical aspects of the valve snap and valve closure responses in the giant scallop Placopecten magellanicus. II. Biochemistry. J. Comp. Physiol., Vol. 137, pp. 105-114.

UTILIZATION

OF SCALLOP’S APPENDIX

Mean dry weight and proximate

(A) First-year Date

9122 10122 1 l/26 l/l 213 3113 4116 5116 6121 7119

l/l 213 313 4116 5116 6121 7119

composition of scallop tissue components as % of dry weight) at Flax Pond.

Adductor

(protein,

carbohydrate

and lipid

Gonad

muscle

%P

%C

%L

%ash

DW

%P

%C

%L

%ash

42.28 211.85 329.82 471.36 436.96 427.66 397.68 348.61 308.79 371.26

70.97 67.80 66.72 62.39 65.93 67.26 75.54 70.79 69.77 65.31

20.10 21.32 20.10 18.17 18.31 18.44 20.35 23.41 23.48 20.21

13.42 14.45 15.32 15.41 16.00 17.21 18.22 5.20 8.21 10.23

26.05 11.81 11.51 11.20 10.49 10.38 11.87 12.97 19.44 12.89

5.48 25.82 57.20 77.85 14.99 66.83 68.85 275.47 375.36 202.77

48.84 62.18 55.58 50.87 52.66 55.27 52.76 68.50 65.77 63.92

10.17 16.65 14.71 14.00 14.36 14.21 14.31 14.55 12.21 12.00

4.01 10.21 10.21 10.65 10.25 10.00 9.87 10.00 8.75 8.61

28.57 28.67 28.67 31.85 37.19 35.36 25.03 17.81 35.39 41.11

Digestive

gland

Other

DW

%P

%C

%L

%ash

DW

%P

%C

%L

%ash

20.61 70.98 131.52 182.36 172.09 146.67 143.03 184.19 204.20 213.33

48.26 54.46 58.15 57.00 53.07 56.07 56.57 56.01 54.21 54.15

20.81 20.62 21.33 20.26 20.31 19.22 20.11 21.05 22.4 1 23.46

10.46 10.95 11.10 10.15 10.10 9.73 10.20 10.68 11.71 12.01

18.98 22.12 18.33 18.58 20.21 23.49 21.27 19.08 20.83 19.92

58.21 214.85 347.06 453.08 440.9 1 403.11 431.88 406.03 443.23 462.15

50.83 52.63 57.92 53.69 49.59 54.19 52.63 54.73 52.53 52.59

6.21 20.12 21.89 20.71 20.10 20.30 19.31 19.75 18.20 18.35

2.70 8.72 9.55 9.01 9.35 9.62 8.96 8.21 8.11 8.55

36.85 34.58 31.92 32.85 31.79 30.98 36.49 33.96 35.39 41.11

cohort Adductor

muscle

Gonad

DW

%P

%C

%L

%ash

DW

%P

%C

%L

%ash

682.89 934.78 1086.35 1037.98 945.78 944.87

67.44 61.97 64.88 67.16 63.58 73.89

29.40 29.11 29.05 28.21 27.65 26.32

10.84 11.21 10.10 9.80 9.00 8.00

17.08 12.90 13.66 11.10 10.92 10.69

94.26 164.78 179.54 198.40 204.39 168.86

50.55 52.6 1 64.55 64.32 49.76 59.39

19.23 20.61 16.21 17.27 16.81 16.81

2.11 3.82 2.40 2.10 3.00 3.00

38.14 29.61 34.65 30.17 27.23 24.70

Digestive

Date

9122 1o/22 1 l/26 l/l 213 3113

I

DW

(B) Second-year Date

9122 IO/22 1 l/26 l/l 213 3/13

135

RESERVES

cohort

Date

9122 10/22 1 l/26

ENERGY

gland

Other

DW

%P

%C

%L

%ash

DW

%P

%C

%L

%ash

207.46 315.29 319.74 363.27 328.10 292.97

51.77 52.19 53.77 54.11 53.5 1 61.25

20.50 10.68 10.45 10.91 10.21 10.06

10.44 9.77 9.10 9.62 9.85 10.00

28.44 22.91 19.44 19.57 20.81 19.85

527.48 774.95 839.85 903.87 808.17 774.04

46.51 60.56 53.82 61.83 52.37 56.09

20.18 10.21 10.01 10.13 10.65 10.75

10.25 9.80 9.76 10.00 10.38 10.99

36.83 35.40 30.83 32.55 28.85 29.15

136

J. EPP ET&. APPENDIX II

Mean dry weight and proximate

(A) First-year Date

lo/29 12/3 l/8 2113 3120 4122 5124 6112

Adductor

and lipid

Gonad

muscle

%P

%C

%I-

%ash

DW

%P

%G

%I-

%ash

253.37 235.62 267.59 152.72 215.30 338.46 159.17 161.58

70.01 65.15 60.90 63.22 66.93 69.51 76.73 77.49

20.47 19.86 19.55 20.47 19.55 22.58 24.89 25.46

14.98 16.87 16.98 17.68 19.42 19.37 7.87 8.27

10.32 12.82 10.45 11.90 12.31 13.25 16.56 14.78

4.23 40.32 42.41 29.72 34.62 100.13 209.55 222.5 1

50.48 57.94 50.87 52.3 1 56.23 61.45 67.14 67.24

17.86 15.68 17.32 16.69 14.99 15.99 15.87 12.87

11.32 10.25 11.25 10.98 12.03 10.88 11.65 9.75

29.81 28.67 31.85 37.19 35.36 25.03 13.17 13.79

Digestive

Other

gland

DW

%P

%G

%I-

%ash

DW

%P

%C

%I

%ash

123.60 100.07 126.05 81.39 91.78 154.66 112.94 131.82

58.46 54.75 56.52 56.10 56.20 74.76 58.81 55.07

23.41 23.78 24.10 22.35 21.22 22.36 22.36 22.89

11.68 11.74 12.14 11.87 10.65 11.36 12.47 12.36

18.98 20.04 18.22 20.64 21.72 19.25 22.85 17.76

316.53 274.02 352.24 231.02 249.97 345.24 237.04 258.69

51.19 50.65 50.64 53.01 54.06 51.71 52.00 52.10

21.44 22.99 25.87 21.87 21.65 20.69 22.10 19.68

9.87 10.69 10.36 10.69 11.97 9.58 9.68 9.65

36.85 33.56 35.55 38.22 33.89 32.31 36.64 38.16

cohort Adductor

Gonad

muscle

DW

%P

%C

%I-

%ash

DW

%P

%C

%I

%ash

853.03 755.49 893.11 764.86 709.72

72.53 67.08 70.88 75.11 83.81

32.10 31.58 30.69 32.22 28.55

14.98 14.25 10.68 11.69 9.80

11.95 13.80 12.84 13.52 15.79

151.13 191.96 203.00 126.52 107.09

50.14 57.90 57.36 57.80 58.08

20.11 18.98 19.25 17.98 17.69

5.68 5.43 5.21 3.87 4.25

32.08 37.06 36.44 32.88 33.36

Digestive

Date

lo/29 1213 l/8 2113 3120

carbohydrate

DW

(B) Second-year Date

lo/29 1213 l/8 2113 3/20

(protein,

cohort

Date

lo/29 1213 l/8 2113 3120 4122 5124 6112

composition of scallop tissue components as % of dry weight) at Southold.

gland

Other

DW

%P

%G

%I

%ash

DW

%P

%C

%I

%ash

308.88 330.97 338.01 288.98 235.37

55.91 47.91 50.43 51.20 53.50

12.65 12.54 11.87 13.65 11.28

10.36 10.54 12.54 10.87 12.65

21.72 19.38 22.90 20.82 23.13

749.62 849.16 846.34 794.92 685.45

55.54 57.94 51.91 52.75 56.40

11.65 11.12 12.36 14.25 12.04

11.68 11.54 12.35 12.69 12.34

32.81 37.10 32.63 31.89 33.81