An energy budget for a Macoma balthica (mollusca) population living on a tidal flat in the Dutch Wadden Sea

Netherlands Journal of Sea Research 19 (1): 84-92 (1985)

AN ENERGY BUDGET FOR A MACOMA BALTHICA (MOLLUSCA) POPULATION LIVING ON A TIDAL FLAT IN THE DUTCH WADDEN SEA

H. HUMMEL* Netherlands Institute for Sea Research. P.O. Box 59, 1790 AB Den Burg, Texel, The Netherlands

ABSTRACT Seasonal and annual energy budgets were compiled for individuals and for a tidal flat population of Macoma balthica in the western part of the Dutch Wadden Sea, based on independent estimates of their numbers, biomass, food consumption and absorption, production and respiration. The consumption of food reached a maximum in late winter and remained high during spring. The absorption of food was maximal in spring and minimal in autumn and early winter. The absorption of food related to chlorophyll a was high only during April, May and June. The respiration was high during spring and summer and reached a minimum in winter. Somatic growth and gonad output were high only in the months April, May and June, whereas during the remainder of the year Macoma lost weight. Indeed, estimates for the absorption of chlorophyll a related food minus respiration were only high during the three months. The production of Macorna appears to depend primarily on the concentration of chlorophyll a related food in the water. The maintenance ration on basis of total consumption amounted to 1.3% of the body weight per day or, when based on the absorbed chlorophyll a related food to 0.4%. The net growth efficiency was 19% on the basis of all absorbed food, and 28% on the basis of chlorophyll a related food. 1. INTRODUCTION In the course of a c o n t i n u i n g study on M a c o m a b a l t h i c a , one of the most common primary con-

sumers in the Dutch Wadden Sea (BEUKEMA, 1976), estimates for food c o n s u m p t i o n and absorption (HUMMEL, 1985a), production (BEUKEMA, personal communication), including gametogenesis (DE WILDE & BERGHUIS, 1977), and respiration (DE WILDE, 1975) have been determined independently. As a preliminary towards constructing a dynamic model of the processes linking these avenues of energy intake and output, it is essential to assemble an energy budget to test if the various data sets are congruent. In particular, alternative estimates for the key parameter of assimilation have been calculated and it will be the primary aim of this paper to decide which of these should be considered most suitable to use as an input for an ecological model on the role of M a c o m a in the energy flow in the Wadden Sea. A c k n o w l e d g e m e n t s . - - T h a n k s are due to Dr. J.J. Beukema for his guidance and support of this study as well for placing at my disposal unpublished data on the seasonal growth of M a c o m a b a l t h i c a . Thanks are given Drs G.C. Cad6e, P.A.W.J. de Wilde, J.J. Zijlstra and R.H. Drent for critically reading the manuscripts. 2. MATERIALS An energy budget for an animal specimen or population can be written as C = P + R + G + F where C = consumption, P = somatic production, R = respiration, G = gonad output and F = faeces, here including excreta (U) (CRISP, 1971). In this paper for the c a l c u l a t i o n s of these values estimates for monthly averages will be used, expressed in kJ.m -2. The budget is calculated for M a c o m a of the Balgzand population

* Present address: Delta Institute for Hydrobiological Research, Vierstraat 28, 4401 EA, Yerseke, The Netherlands

ENERGY BUDGET FOR MACOMA

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with a mean standing stock of adult (1 year and older) animals of 40.5 kJ.m -2 (converted from BEUKEMA,1981a) or 60 animals per m 2 (BEUKEMA, 1980). The mean submersion period of the tidal flats at Balgzand has been fixed at 7 hours, the emersion period at 51/2 hours. It is assumed that 1 gram of ash free dry weight of body tissue equalled 18.0 to 19.5 kJ (BEUKEMA & DE BRUIN, 1979; taking values of 4.3 to 4.75 kcal.g -1 for physiological oxidation). Further 1 ml 02 is considered equal to 20.1 J (CRISP, 1971) and 1 g C of ingested food equal to 47.8 kJ (PLATT & IRWIN, 1973). Other basic data used in the calculation of the energy budget are compiled in Table 1. The consumption of organic carbon (C) is calculated from the observed chlorophyll a intake (HUMMEL, 1985a; calculated from stomach contents and thus excluding possible pseudofaeces) using the observed carbon to chlorophyll a ratios of the suspended material in the water and in the sediment (HUMMEL, 1985a). It is assumed that Macoma does not select its food on the basis of food quality or size (GILBERT, 1977; HARGRAVE, 1978), although particles taken in from the water might be slightly under estimated (HUMMEL, 1985a). The carbon to chlorophyll a ratio in the water measured by routine sampling had to be corrected with a factor 1.1 (1/0.9) to obtain the mean value for a submersion period (HUMMEL, 1985a). An alternative way to estimate C was used also, viz. by multiplying the observed amounts of chlorophyll a (Cc) taken in by fixed factors of 143 for food from the water and 91 for food from the sediment. These arbitrary factors are the means of the carbon to chlorophyll a ratios observed at Balgzand during the growing season (April, May, June) (HUMMEL, 1985a), and are used to convert values for chlorophyll a in algal and algae associated material to carbon values. Account has been taken of the amounts of food taken in from the overlying water colomn or the bottom sediment. The two phases of the tidal cycle were quantified separately. During submersion 78% of the intake originated from the water, the remaining 22% and the intake during emersion originated from the sediment (HUMMEL, 1985a). The actual amounts of food absorbed (A = C - F and Ac = C c - F) were calculated from C (all food) or Cc (chlorophyll a related food) and the absorption efficiency. The absorption efficiency in the growing season (April, May, June) was 56% and during the remainder of the year 35% (HUMMEL, 1985a).

86

H. HUMMEL

Monthly values for biomass and somatic production (P) were calculated from data kindly provided by Dr. J.J. Beukema (personal communication, see also fig. l b in BEUKEMA & DE BRUIN, 1977). Annual gonad output (G) has been calculated as 24.1% of the standing stock in spring, viz. the average of the values for March, April and May (DE WILDE & BERGHUIS, 1977). The values for respiration (R) have been calculated from figures given by DE WILDE (1975), taking into account seawater temperature (monthly mean water temperature at Breezanddijk; obtained from the "Rijksinstituut voor Visserijonderzoek" IJmuiden) and time spent on deposit and suspension feeding or rest (HUMMEL, 1985a). For the times spent on the several feeding activities it was assumed that April, May and July were similar to June and that January and February were similar to December. The expected production, i.e. the "scope for growth", throughout the year was calculated by subtracting the values for respiration from those for the absorbed food (A - R and Ac - R). The annual gross (K1) and net growth efficiency (K2) were calculated respectively as (P + G)/C and (P + G)/A. Similarly, monthly Kc 2 values were calculated as (P + G)/Ac. 3. RESULTS AND DISCUSSION 3.1. MONTHLY VALUES FOR COMPONENTS OF THE ENERGY BUDGET Monthly values for the components of the energy budget, shown in Table 2 and in Fig. 1, clearly point to seasonal variation. The total consumption (C; Fig. la) reaches its maximum in late winter and remains at a high level during spring and early summer. During late summer the consumption drops drastically, reaching a minimum in early winter. The maximum for the consumption of chlorophyll a related food (Cc; Fig. lb) is mainly restricted to the months April, May and June. During the remainder of the year the consumption of chlorophyll a related food is low. The origin of the food consumed is known from the analysis of the stomach content described in HUMMEL (1985a) and recapitulated in Table 1. As shown in Fig. 1, both the total food consumed (C) and the chlorophyll a related food consumed (Cc) originated for the greater part from the water colomn (81% of C and 76% of Cc) and only for a minor part from the bottom sedi-

ment, as deduced indirectly from the stomach analysis. Because Cc was calculated with a fixed factor (see section 2) it may be higher than C. The absorbed food (A) reaches its maximum only in spring (Fig. lc). The difference between the maximum observed for C in February and March is caused by a lower absorption efficiency (35%) during these months as compared to the 3 following months (56%) (HUMMEL, 1985a). The maximum for the absorbed chlorophyll a related food (Ac)is again more pronounced and restricted to the months April, May and June (Fig. lc). The large differences between the high values in spring and the low values during the remainder of the year will mainly be caused by the large seasonal fluctuations of the chlorophyll a concentrations in the water (HUMMEL, 1985a), rather than by fluctuations in the absorption efficiency. The respiration (R; Fig. l d ) i s low in the winter and due to higher values for temperature, mean weight and feeding activity (Table 1), rises during spring to a broad maximum lasting from spring to early autumn. 3.2. THE "SCOPE FOR GROWTH" The production observed in the field (P + G; Table 2) was high only during the months April, May and June (Fig. 2a). From July up to February Mac o m a steadily looses weight (BEUKEMA & DE BRUIN, 1977), i.e. the energy balance is negative. When "scope for growth" is estimated from the total ingested food minus respiration (A - R in Fig. 2b) a large discrepancy emerges. In partickJ m d

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Fig. 1. Basic data for (a) total consumption (C), and (b) consumption of chlorophyll a related food (Cc) originating from the bottom sediment (O) or the water column (0)+ (c)absorption (A) and amounts of absorbed chlorophyll a related food (Ac) and (d) the respiration (R) for a Macoma individual on Balgzand. All data in kJ.ind- 1.month i

ENERGY BUDGET FOR MACOMA

87

TABLE 2 The monthly values for consumption (C), absorption (A), the chlorophyll a related consumption (Cc) and absorption (Ac), positive and negative somatic production by growth or weight loss (P), gonad output (C), respiration (R) and net growth efficiency (Kc 2 = (P + G)/Ac) for a "mean" individual of the 1 + year old population of Macoma balthica on Balgzand (expressed in energy units kJ, except for Kc2). See Materials for definitions and calculation procedures, and Table 1 for basic data. Month

C

A

Cc

Ac

P

G

R

January February March April May June July August September October November December

0.22 0.55 0.78 0.45 0.52 0.40 0.53 0.29 0.17 0.17 0.07 0.16

0.08 0.19 0.27 0.25 0.29 0.22 0.19 0.10 0.06 0.06 0.03 0.06

0.07 0.08 0.20 0.39 0.64 0.40 0,30 0.10 0.15 0.08 0.07 0.06

0.02 0.03 0.07 0.22 0.36 0.22 0.11 0.04 0.05 0.03 0.02 0.02

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0 0 0.04 0.04 0.05 0 0 0 0 0 0 0

0,01 0.01 0.02 0.04 0.08 0.13 0.13 0.14 0.14 0.10 0.05 0.02

Annual total

4.31

1.80

2.54

1.19

0.19

0.13

0.87

ular, the high e s t i m a t e s for c o n s u m p t i o n and abs o r b e d f o o d d u r i n g F e b r u a r y and M a r c h are not

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Fig. 2. The (a) production (P + G; kJ.ind-1; El) of Macoma in the field and (b) t h e " s c o p e for growth"(kJ.ind-1) as calculated from all absorbed food (A - R; ©) and from the absorbed chlorophyll a related food (Ac - R; I).

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+ + + + -

1.6 1.4 0.6 0.9 0.9 0.9 0.6 2.2 1.3 1.9 2.1 1.9

r e f l e c t e d in the p r o d u c t i o n ( g r o w t h ) e s t i m a t e s for t h e s e m o n t h s . This p o o r fit w i t h p r o d u c t i o n w h e n the " s c o p e for g r o w t h " is b a s e d on all a s s i m i l a t ed f o o d (A - R) m a y be c a u s e d by a r e l a t i v e l y high p e r c e n t a g e of p o o r l y d i g e s t i b l e d e t r i t u s in the f o o d d u r i n g t h e s e m o n t h s . O l d e r d e t r i t u s is t h o u g h t to be of l o w n u t r i t i v e value (FENCHEL, 1972; FENCHEL & J(~RGENSEN, 1977). AS w a s previo u s l y s h o w n , p a r t i c u l a r l y d u r i n g the m o n t h s m e n t i o n e d , the r a t i o of c h l o r o p h y l l a to o r g a n i c c a r b o n w a s l o w in t h e o v e r l y i n g w a t e r (HUMMEL, 1985a). On the o t h e r h a n d " s c o p e for g r o w t h " as c a l c u l a t e d f r o m t h e net d i f f e r e n c e b e t w e e n t h e o b s e r v e d c h l o r o p h y l l a r e l a t e d f o o d and t h e r e s p i r a t i o n (Ac - R in Fig. 2b) i n d i c a t e s t h a t r a p i d g r o w t h is r e s t r i c t e d to the m o n t h s April, May and June, w h i c h c o i n c i d e s w i t h the observed p r o d u c t i o n (Fig. 2a). The fit of " s c o p e for g r o w t h " (Ac - R) w i t h a c t u a l p r o d u c t i o n (P + G) is fair for all m o n t h s : none of the p o i n t s so derived (filled s q u a r e s in Fig. 3) d e v i a t e s far f r o m the line of e q u a l i t y . N e g a t i v e v a l u e s for both Ac - R and P + G w e r e o b s e r v e d for s u m m e r and aut u m n w i t h v a l u e s c l o s e to zero in w i n t e r . The w e i g h t l o s s e s o b s e r v e d in s u m m e r and early a u t u m n w e r e h i g h e r than d u r i n g late aut u m n and w i n t e r as a result of h i g h e r r e s p i r a t i o n rates, c a u s e d by h i g h e r t e m p e r a t u r e s as well as h i g h e r m e a n w e i g h t s and f e e d i n g a c t i v i t i e s during s u m m e r and early a u t u m n . The h i g h e r ( d e p o s i t ) f e e d i n g a c t i v i t y o b s e r v e d d u r i n g Sept e m b e r m a y be a r e s p o n s e to the l o w c o n c e n t r a -

88

H. HUMMEL

tion of chlorophyll a in the water (HUMMEL, 1985a). This extra deposit feeding activity amounted to about 18% of the total available time (Table 1) and would result in an extra intake by the Macoma population during September of 0.027 kJ.ind-1, when expressed as total food assimilation (A), or 0.022 kJ.ind - 1, when expressed as chlorophyll a related food assimilated (Ac). However, this extra deposit feeding activity, a more costly activity than suspension feeding (Table 1), would cost 0.033 kJ-ind -1. Thus, the extra deposit feeding activity during September is not expected to have resulted in a net gain of energy, but in a net energy loss. During the following months the balance between a gain in energy from food and loss in energy from the extra activity would be more and more negative at high feeding activities, because of a declining yield from the food intake as a result of lowering concentrations of food (HUMMEL, 1985a). Apparently, the response of Macoma to reduce their feeding activities to low levels as observed during winter is an advantageous one (Table 1, HUMMEL, 1985a).

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3.3. THE GROWTH EFFICIENCY Because the values for "scope for growth" as calculated from the chlorophyll a related food (Ac - R) fitted best with the observed values for production (P + G), the net growth efficiency has been calculated only on the basis of the absorbed chlorophyll a related food (Table 2; Kc2). As one would expect, the obtained values for net growth efficiency depend on the amounts of food absorbed (Fig. 4). Similar relationships have been found for Mytilus edulis (THOMPSON & BAYNE, 1974; WINTER & LANGTON, 1976; WIDDOWS, 1978b; BAYNE & WIDDOWS, 1978). The net growth efficiency yielded negative values below an absorption of about 0.09 k J . m o n t h - l . i n d -1, which is equivalent to a monthly absorption of chlorophyll a related food of about 11% of the body weight or a daily absorbed ration of about 0.4% of the body weight. Maintenance rations are given mostly on the basis of total amount of food ingested (C), so the above value should be divided by the mean absorption efficiency (Ac/C = 0.28; Table 3) resulting in a daily maintenance ration of 1.3%. The latter value is almost identical to that found for Macoma in the laboratory (1.2%; HUMMEL, 1985b) and within the range of those observed in Mytilus edulis (1.1 to 5%; THOMPSON & BAYNE, 1974; WINTER & LANGTON, 1976; WIDBOWS, 1978b; BAYNE & WlDDOWS, 1978). Most of the individual monthly values for Kc 2

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Fig. 3. The relation between the production (P + G) in the field (abscissa) and the "scope for growth" (ordinate) as calculated from all absorbed food (A - R; O) and from the absorbed chlorophyll a related food (Ac - R; I ) . All data in kJ.ind-l.month -1. The solid line represents the best fitting line for the "Ac - R" data; the broken line indicates the position the points should have taken when calculated "scope for growth" exactly equalled the observed production.

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ENERGY BUDGET FOR MACOMA

closely fit the usually observed relationship with ration of food absorbed. The deviant position of the values for Kc 2 for March and July (Fig. 4) may be caused by the fact that respiration during March is still low, whereas during July a great part of the energy from the intake is dissipated by respiration (Table 2). These two odd values represent exactly the 2 months during which the energy balance changed from negative to positive values and vice versa. 3.4. THE ANNUAL ENERGY BUDGET FOR A MACOMA BALTHICA POPULATION The values for the annual energy budget (Table 3) were obtained by summing monthly values. The individual values were converted to values for the population of 1+ year old Macoma on Balgzand, which on an average consisted of 60 such individuals per m 2 (BEUKEMA, 1980). The values obtained can be compared with similar estimates for some other tellinid bivalves, also included in Table 3. The energy budget for Macoma as shown in the top 2 lines of Table 3 can be balanced in either of the two ways shown. When the absorption is calculated from A -- P + G + R and the value for respiration is taken from the results of DE WILDE (1975), a value for absorption (A) of 71.7 kJ.m -2 is obtained (Table 3). The absorption value calculated independently from the total consumption, multiplied by the absorption efficiency, would amount to 107.4 kJ.m -2 (Table 3). The former value for A t u r n s out to be close to the values for absorbed chlorophyll a related food; 60ind-m --2 x 1.19 kJ.ind -1 = 71.4 kJ.m - 2 ( T a . ble 2). This remarkably close fit suggests that energy used by Macoma is based on the utilization of chlorophyll a related food only. This conclusion has been drawn already from the above (Figs 2 and 3) observed better fit between the monthly values for observed production in the field with those for the "scope for growth" on the basis of the absorbed chlorophyll a related food only, in contrast to the fit on the basis of all absorbed food. Thus, the value for A of 107.4 kJ.m -2, including all organic carbon, is probably too high. When calculating this value it was assumed that food is absorbed as it is present in the environment, i.e. the carbon to chlorophyll a ratio was assumed to be the same in the ambient food, the absorbed food, as well as in the faeces. However, part of the carbon that is not associated with chlorophyll a may not have been assimi-

89

lated, resulting in an overestimate for the absorption. Therefore, I would suggest that the same values for the ratio of chlorophyll a related food and chlorophyll a of the bottom and water can be used throughout the year. These values equal those observed for the April, May and June period (see section 2) and amount to 143 for the water and 91 for the top layer of the sediment. The main food for Macoma then would consist of algae, "fresh" algal detritus and closely associated micro-organisms. Excretion (U, in our computations included with faeces as part of the rejecta) is thought to be quantitatively of little importance in the energy budget, in Mytilus edulis the excretion was found to amount to only 12% of the respiration (BAYNE, 1973; E}AYNE & WIDDOWS, 1978) and in Mytilus chilensis to only 3% of the assimilated ration (NAVARRO & WINTER, 1982). In Macoma excretion would then presumably be maximally 8 kJ.m -2, not significantly contributing to the difference between the 2 estimates of absorption (71.7 and 107.4 in Table 3). When the annual value of 71.7 kJ.m -2 for absorbed food is taken for granted, only 28% of the consumed food (257.7 kJ.m -2) is actually used. Thus, on an annual basis, only 28% of the food ingested was really assimilated. In Scrobicularia plana higher percentages were assimilated (Table 3). As is depicted in Fig. 5, the low assimilation efficiency in Macoma may be caused by the intake of an inert component in the consumed food (C - Cc) which has little or no nutritional value to Macoma and is without a direct relation to the chlorophyll a related food (Cc). The ultitotal intake ~258~

unsuitable 106 as food (C-Co)

F ~86

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suitable as food (Co

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respiration production

Fig. 5. Schematic model of the main pathways in the energy budget for a mean population of 60 1 + year old Macoma on a tidal flat in the Dutch Wadden Sea. All values are in kJ-m 2.y-1; explanation in the text.

90

H. HUMMEL

TABLE 3 Annual values for populations of tellenid bivalves for consumption (C; kJ-m-2), absorption efficiency (A/C), absorption (A; kJ.m-2), somatic production (P; kJ.m- 2), gonad output (G; kJ-m-2), respiration (R; k J-m- 2), gross (K1) and net growth efficiency (K2), number (n; m -2) and biomass (B; kJ.m 2). Values between brackets are not directly estimated but calculated from e.g. A = P + G + Ror R --- A - P - G. Data forMacoma are calculated for a population of on average 60 1 + year old individuals. Explanation: a. A is calculated from results given by HUMMEL (1985a) (Table 1) and R = A - P - G. b. R is calculated from results given by DE WILDE (1975) (Table 1) and A -- R + P + G. c. Low level, d. High level, e. Tellinagrund. f. Fine sand center. C Macoma balthica

Western Wadden Sea This study Scrobicularia p l a n a

North Wales HUGHES (1970)

a* b*

257.7

c* d*

3565.7 436.6

A/C

0.35-0.56 (0.28) (0.71) (0.69)

A

P

107.4 (71.7)

12.6 12.6

G

7.8 7.8

R

K1

K2

n

B

(87.0) 0 . 0 8 51.3 0 . 0 8

0.19 0.28

60 60

48.1 48.1

(2514.0) 2 5 1 . 4 268.2 1994.4 0.15 (302.1) 55.7 17.6 2 2 8 . 8 0 . 1 7

0.21 0.24

150 55

855.6 81.3

Tellina fabula

e*

German Bight SALZWEDEL (1980)

f*

(148.8) (216.5)

63.2 51.1

4.8 25.9

80.8 139.5

0.46 0.36

987 980

39.2 83.4

1966 1967 1968

(186.9) (84.4) (111.9)

27.6 4.3 14.7

2.7 7.1 17.4

156.6 73.0 79.8

0.16 0.14 0.29

111 59 47

74.9 59.7 56.6

Tellina tenuis

N.W. Scotland TREVALLION (1971)

mately assimilated food (Ac) is derived from the actual intake of chlorophyll a related food (Cc) (Fig. 5). The production (P + G) in M a c o m a amounted to 28% of the assimilated chlorophyll a related food (Ac) (Kc2, Table 3). Of course the gross growth efficiency on the basis of total consumption (K1) is much lower, viz. only 8%. The values for c o n s u m p t i o n (C), absorption (A), production (P and G) and respiration (R) of M a c o m a are all w i t h i n the range of those found for the other tellinid bivalves after making allowance for the difference in biomass of the respective populations (Table 3). 3.5. THE MAIN CAUSES OF FLUCTUATIONS IN PRODUCTION From the preceding sections it is clear that the production of M a c o m a will be primarily governed by the availability, i.e. concentration, of chlorophyll a related food in the water. The observed production, best resembled the monthly changes in the "scope for g r o w t h " as calculated from the absorbed chlorophyll a related food (Figs 2 and 3). Consequently, in the annual energy budget, the absorption value calculated from the directly measured production (P + G) and respiration (R) fitted best with the absorption value of chlorophyll a related food (Table 2).

In addition, in the laboratory growth was more rapid at higher concentrations of suspended algae, up to 7 mg C.1-1 (HUMMEL, 1985b). Under these experimental c o n d i t i o n s at a given concentration of algae, the growth remained the same during all seasons. Also in the field data, the year-to-year variation in growth rates of M a c o m a was found to be positively correlated with the year-to-year variation in primary production (BEUKEMA et al., 1977), though in this case the primary production of the benthic microfauna was measured. If, for the main food source, i.e. the overlying water, a constant factor of 143 is assumed for the ratio of chlorophyll a related food (in mg C.1-1) and chlorophyll a (in m g . t - 1), the monthly concentration of the food in the water will on average amount to 3.0 mg C.1-1 in spring and to values invariably below 1 mg C-I-1 during the remainder of the year (HUMMEL, 1985a). HUMMEL (1985b) showed that in the laboratory M a c o m a lost weight at concentrations of suspended algae lower than about 1.3 mg C-I- 1. From this observation in the laboratory, consistent weight loss in the field may be expected during all seasons except spring and this indeed has been observed (Fig. 2; BEUKEMA & DE BRUIN, 1977). However, in other areas with differing food conditions, M a c o m a may behave otherwise, be-

ENERGY BUDGET FOR MACOMA

cause it can utilize both suspension and deposit feeding (HUMMEL, 1985a). Therefore, given other feeding strategies Macoma may show quite different seasonal patterns in the energy budget as given here for the Dutch Wadden Sea. It is striking that the seasonal changes in the chlorophyll a concentration in the water are parallel to changes in the absorption efficiency (HUMMEL, 1985a) and in the percentage chlorophyll a to total carbon (HUMMEL, 1985a). High values in spring of the chlorophyll a concentration coincide with high values for the absorption efficiency and percentage chlorophyll a to carbon, whereas low values coincide in the remainder of the year. Moreover, the water clearance rate (filtration rate) in the field (HUMMEL, 1985a), as well as in the laboratory (HUMMEL, 1985b), and the deposit feeding activity (HUMMEL, 1985a) showed seasonal changes. Intermediate rates and activities were reached during spring, higher values during summer and low values during autumn and winter. In addition, the formation of gametes shows a parallel seasonal cycle starting in July and ending approximately in March (LAMMENS, 1967; DE WILDE & BERGHUIS, 1977). DE WILDE & BERGHUIS (1977) thought temperature to be the main triggering factor for the start and end of this reproductive cycle. It cannot be decided which factor is actually triggering the seasonal changes: temperature, food availability or gonadal state. As HUMMEL (1985a) reasoned, the relatively high absorption efficiency observed during spring may be caused by the high concentration of assimilable food, i.e. a high concentration, absolute and relative, of chlorophyll a related food. The higher water clearance rate during summer, coincident with a higher deposit feeding activity, may be a response to the lower concentration of assimilable food in the water (HUMMEL, 1985a). The high costs of respiration, resulting from this extra feeding activity, together with a lowering gain from the food intake, as a consequence of diminishing concentrations of available food, may be the reason why Macoma soon stops this high level of activity, resulting in low feeding activities during the autumn and winter. However, it is not clear whether all these parallel changes are triggered by changes in food concentration and food composition or by internal physiological changes such as the reproductive cycle, which in its turn could be influenced directly or indirectly by temperature. At any rate, from this study it is clear that changes

91

in the intake of food and in the energy budget of Macoma balthica in the Dutch Wadden Sea can be explained largely by changes in the concentration of chlorophyll a related food. Therefore, it is possible that in the course of evolution, in order to achieve an economical use of the available energy, all the changes mentioned were arrived at in parallel. Attempting to designate a primary cause for one of these changes may then result in the "chicken and egg"-enigma: "which one came first?" 3.6. IMPLICATIONS FOR THE WADDEN SEA FOOD CHAIN Food in the form of organic matter in general is often thought to be plentiful for the primary consumers living in the western Dutch Wadden Sea. However, for Macoma it is shown above that probably only the chlorophyll a related food results in any production, and that the production of Macoma is limited by the concentration of such food. If such a limitation of the production would apply to all primary consumers, it could, in turn, also indirectly limit the secondary consumers (predators) in the Wadden Sea, because this last group may be food limited by the production of the primary consumers (BEUKEMA, 1981 b). The primary consumers living on the tidal flats of the Wadden Sea are to a lesser extent suspension feeders, and to a lesser extent deposit feeders (BEUKEMA, 1976). Macorna may be regarded as representative for the group of benthic consumers as a whole, since it takes 3/4 of the food from the water and 1/4 from the sediment. In addition, the growth efficiency of Macoma (0.28; Table 3) is within the range quoted for other marine primary consumers (BEUKEMA, 1981b). The production of the large (multicellular) primary consumers in the Wadden Sea is estimated at 50 g ADW.m-2.y -1 (BEUKEMA, 1981b), consequently their minimal absorption of food would be 50•0.28 or about 180 g ADW, almost exclusively in the form of chlorophyll a rich algae and closely related material. Roughly 3/4 or 135 g ADW.y -~ would be taken from the water and 1/4 or 45 g ADW.y-1 from the sediment. On the tidal flats the average primary production was found to amount to 325 g ADW-m - 2 . y - 1 on the bottom, and in the water above these flats to only 50 g ADW-m-2.y -1 (CADI~E & HEGEMAN, 1974; CADI~E,1980). Thus, for the smaller group of deposit feeders food appears to be unlimited.

92

H. HUMMEL

H o w e v e r , t h e p r o d u c t i o n of t h e l a r g e r g r o u p of s u s p e n s i o n f e e d e r s w i l l d e p e n d l a r g e l y on t h e c o n c e n t r a t i o n of a l g a e p r o d u c e d e l s e w h e r e , viz. e i t h e r t r a n s p o r t e d by t h e t i d a l c u r r e n t s to the t i d a l f l a t s or w h i r l e d up f r o m the b o t t o m (HUMMEL, 1985a). Indeed, e v i d e n c e is a v a i l a b l e t h a t i m p o r t of o r g a n i c m a t e r i a l f r o m t h e c o a s t a l a r e a s of t h e N o r t h Sea and t h e m a i n t i d a l c h a n n e l s t o w a r d s t h e t i d a l f l a t s can be high (CADI~E, 1980; HUMMEL, 1985a). 4. REFERENCES

BAYNE, B.L., 1973. Physiological changes in Mytilus edulis L. induced by temperature and nutritive stress.--J, mar. biol. Ass. U.K. 53: 39-58. BAYNE,B.L. & J. WIDDOWS, 1978. The physiological ecology of two populations of Mytilus edulis L.-Oecologia 37: 137-162. BEUKEMA,J.J., 1976. Biomass and species richness of the macrobenthic animals living on the tidal flats of the Dutch Wadden Sea.--Neth. J. Sea Res. 10: 236-261. , 1980. Calcimass and carbonate production by molluscs on the tidal flats in the Dutch Wadden Sea. I. The tellinid bivalve Macoma balthica.-Neth. J. Sea Res. 14: 323-338. ,1981a. Quantitative data on the benthos of the Wadden Sea proper. In: N. BANKERS, H. KOHL & W.J. WOLFF. Ecology of the Wadden Sea, I. Balkema, Rotterdam: 134-142. - - - - , 1981b. The role of the larger invertebrates in the Wadden Sea ecosystem. In: N. BANKERS,H. KOHL & W.J. WOLFF. ECology of the Wadden Sea, I. Balkema, Rotterdam: 211-221. BEUKEMA,J.J. & W. DE BRUIN, 1977. Seasonal changes in dry weight and chemical composition of the soft parts of the tellinid bivalve Macoma balthica in the Dutch Wadden Sea.--Neth. J. Sea Res. 11: 42-55. - - - - , 1979. Calorific values of the soft parts of the tellinid bivalve Macoma balthica (L.) as determined by two methods.--J, exp. mar. biol. Ecol. 37: 19-30. BEUKEMA,J.J., G.C. CADI~E & J.J.M. JANSEN,1977. Variability of growth rate of Macoma balthica (L.) in the Wadden Sea in relation to availability of food. In: B.F. KEEGAN, P.O'CEIDIGH & P.J.S. BOADEN. Biology of benthic organisms. Pergamon Press, Oxford: 60-77. CADEE, G.C., 1980. Reappraisal of the production and import of organic carbon in the western Wadden Sea.--Neth. J. Sea Res. 14" 305-322. CADEE, G.C. & J. HEGEMAN, 1974. Primary production of the benthic microflora living on tidal flats in the Dutch Wadden Sea.--Neth. J. Sea Res. 8" 260-291. CRISP, D.J., 1971. Energy flow measurements. In: HOLME, N.A. & A.D. MCINTYRE. Methods for the study of marine benthos. IBP Handbook No. 16. Blackwetl Scientific Publications, Oxford, Edinburgh: 197-279. FENCHEL,T., 1972. Aspects of decomposer food chains in marine benthos.--Verh, dt. zool. Ges. 85: 14-23.

FENCHEL, T.M. & B.B. J(~RGENSEN,1977. Detritus food chains of aquatic ecosystems: the role of bacterlB.--Adv. Microbiol. Ecol. 1: 1-58. GILBERT, M.A., 1977. The behaviour and functional morphology of deposit feeding in Macoma balthica (Linne, 1758) in New England.--J. Moll. Stud. 43: 18-27. HARGRAVE,B.T., 1978. Geochemical and biological observations in intertidal sediments from Cobequid Bay, Bay of Fundy, Nova Scotia.--Fish. Mar. Serv., Techn. Rep. 782: 1-43. HUGHES, R.N., 1970. An energy budget for a tidal flat population of the bivalve Scrobicularia plana (da Costa).--J. Anim. Ecol. 39: 357-381. HUMMEL, H, 1985a. Food intake of Macoma balthica (Mollusca) in relation to seasonal changes in its potential food on a tidal flat in the Dutch Wadden Sea.--Neth. J. Sea Res. 19: 52-76. - - - - , 1985b. Food intake and growth in Macoma balthica (Mollusca)in the laboratory.--Neth. J. Sea Res. 19: 77-83. NAVARRO,J.M. & J.E. WINTER, 1982. Ingestion rate, assimilation efficiency and energy balance in Mytilus chilensis in relation to body size and different algal concentrations.--Mar. Biol. 67: 255-266. PLATT, 1". & B. IRWIN, 1973. Caloric content of phytoplankton.--Limnol. Oceanogr. 18: 306-310. SALZWEDEL, H., 1980. Energy budgets for two populations of the bivalve Tellina fabula in the German Bight.--VerEff. Inst. Meeresforsch. Bremerh. 18: 257-287. THOMPSON,R.J. & B.L. BAYNE,1974. Some relationships between growth, metabolism and food in the mussel Mytilus edulis.--Mar. Biol. 27: 317-326. TREVALLION,A., 1971. Studies on Tellina tenuis Da Costa. Ill. Aspects of general biology and energy flow.--J, exp. mar. Biol. Ecol. 7: 95-122. WARWICK, R.M., I.R. JOINT & P.J. RADFORD,1979. Secondary production of the benthos in an estuarine environment. In: R.L. JEFFERIES & A.J. DAVY. Ecological processes in coastal environments. Blackwell Scientific Publications, Oxford, Edinburgh: 429-450. WIDDOWS, J., 1978. Physiological indices of stress in Mytilus edulis.--J, mar. biol. Ass. U.K. 58: 125-142. WILDE, P.A.W.J. DE, 1975. Influence of temperature on behaviour, energy metabolism and growth of Macoma balthica (L.) In: H. BARNES. Ninth European Marine Biology Symposium. Aberdeen University Press, Aberdeen: 239-256. WILDE, P.A.W.J. DE & E.M. BERGHUIS, 1977. Laboratory experiments on the spawning of Macoma balthica; its implication for production research. In: D.S. McLUSKY & A.J. BERRY. Physiology and behaviour of marine organisms. Pergamon press, Oxford: 375-384. WINTER, J.E. & R.W. LANGTON, 1976. Feeding experiments with Mytilus edulis L. at small laboratory scale. I. The influence of the total amount of food ingested and food concentration on growth. In: G. PERSOONE & E. JASPERS. Proceedings of the 10th European Symposium on Marine Biology, 1. Universa Press, Wetteren: 565-581.