The importance of grazing food chain for energy flow and ... · The importance of grazing food chain for energy flow and production in three intertidal sand bottom communities of

HELGOLANDER MEERESUNTERSUCHUNGEN Helgol~nder Meeresunters . 39, 273-301 (1985)

The importance of grazing food chain for energy f low

and production in three intertidal sand bottom

communit ies of the northern Wadden Sea

Harald Asmus & Ragnhild Asmus

Biologische Anstalt Helgoland (Litoralstation]; D-2282 List~Silt, Federal Republic of Germany

ABSTRACT: In three inter t idal sand bot tom communi t ies of the "K6nigshafen" (Island of Sylt, North Sea), the biomass product ion and respirat ion of phytobenthos , phytoplankton, macrozooben- thos, and in situ communi ty metabol i sm were measu red month ly dur ing 1980. The study sites were characterized by different communit ies (Nereis-Corophium-belt, seagrass-bed, Arenicola-flat) and by a h igh a b u n d a n c e of the mollusc Hydrobia ulvae. Benthic dia toms are the major const i tuents of plant biomass in the Arenicola-flat. In this community, gross pr imary productivi ty amounts to 148 g C m-2 a -1 .82 % of this productivity is caused by microbenthos, whereas phy top lank ton consti tutes only 18 %. In the seagrass-bed, gross pr imary productivi ty amounts to 473 g C m -2 a -1. 79 % of this is genera ted by seagrass and its epiphytes, whereas microphytobenthos contr ibutes 19 %. In the Nereis-Corophium-belt, only microphytobenthos is impor tan t for hiomass and pr imary productivi ty (gross: 152 g C m -2 a- l ) . Annua l product ion of macrofauna proved to be similar in the A_renicola- flat (30 g C m -2 a -1) to that in the seagrass-bed (29 g C m -2 a- l ) . Only one third of this amount is produced in the Nereis-Corophium-belt (10 g C m -2 a - l ) . The ma in par t of secondary product ion and animal respirat ion is contr ibuted by grazing H. ulvae. In the seagrass-bed, 83 % of the energy used for production is obta ined from the grazing food chain. In the Arenicola-flat and the Nereis- Corophium-belt, the importance of non-graz ing species is greater. A synchrony of seasonal development of p lant biomass and monthly secondary product ion was observed. In the Arenicola- flat and the seagrass-bed, where densi ty and product ion of macrofauna are high, a conspicuous decrease in biomass of microbenthos occurs dur ing the warmer season, whereas in the Nereis- Corophium-belt primary production causes an increase in microphytobenth ic biomass in summer and autumn. Energy flow through the macrofauna amounts to 69 g C m -2 a -~ in the Arenicola-flat, 85 g C m -~ a -1 in the seagrass-bed and 35 g C m -2 a -1 in the Nereis-Corophium-belt. Based on the assumption that sources of food are used in proportion to thei r availability, 49 g C m -2 a -1 (Arenicola-fiat), 72 g C m -2 a -1 (seagrass-bed) and 26 g C m -2 a -1 (Nereis-Corophium-belt) are est imated as t aken up by the grazing food chain. All three subsystems are able to support the energy requirements from their own pr imary product ion and are not d e p e n d e n t on energy import from adjacent ecosystems.

I N T R O D U C T I O N

I n t e n s e b i o l o g i c a l a c t i v i t y is a p r o m i n e n t f e a t u r e of i n t e r t i d a l a r eas . T i d a l f la t s a r e

e x p o s e d to h i g h l i g h t i n t e n s i t y d u e to l o w w a t e r d e p t h a n d t h e p e r i o d i c e m e r g i n g of t h e

s e d i m e n t . A d d i t i o n a l l y , n u t r i e n t s a r e a b u n d a n t ; t hus , t i d a l f la t s m e e t t h e r e q u i r e m e n t s

for h i g h p r i m a r y p r o d u c t i o n . A c c o r d i n g l y , b e n t h i c s e c o n d a r y p r o d u c t i o n is e n h a n c e d

w h i c h is i n d i c a t e d b y t h e g r e a t b i o m a s s of b e n t h i c m a c r o f a u n a .

L o n g - t e r m m e a s u r e m e n t s of i n t e r t i d a l p r i m a r y p r o d u c t i o n of p h y t o p l a n k t o n a n d

© Biologische Anstal t Helgoland, Hamburg

274 H. Asmus & R. Asmus

microphytobenthos have been conducted chiefly in the Dutch Wadden Sea (Postma & Rommets, 1970; Cad~e & Hegeman, 1974 a,b, 1979; Cad~e, 1980; Gieskes & Kraay, 1975; Colijn & de Jonge, 1984}. Based upon these findings, it was postulated that autochthonous primary production is relatively low and that it only insufficiently explains the richness and high production of the fauna (Van den Hoek et al., 1979; Kuipers et al., 1981). These authors suppose that the input of phytoplankton and detritus from the North Sea builds the main source of food in the Wadden Sea ecosystem.

Macrofauna, rich in biomass, constitutes an important link between primary producers and consumers of higher levels. Macrofauna must necessarily be highly productive in order to maintain the high values of biomass that are found in the Wadden Sea in spite of strong predation by numerous birds, fishes and invertebrates. Measurements of secondary production in intertidal areas reveal values similar to those in subtidal areas (Beukema, 1981; Warwick & Price, 1975). Although the structure of macrofauna has been investigated intensively in the German Wadden Sea, investigations on secondary production are missing. But measurements of secondary production are not sufficient in order to characterize the function of macrofauna in the ecosystem. Energy flow through macrofauna cannot be measured directly, whereas production and respiration of macrofauna can be measured. The latter are the two main constituents of energy flow, which is the sum of both.

Simultaneous measurements of secondary production and respiration were per- formed by studying single populations in order to obtain evidence of their total energy budget (Hughes, 1970; Kuenzler, 1961; Odum & Smalley, 1959; Teal, 1962; Mann, 1965}. The importance of the respiration of macrofauna species could be proved (Hargrave, 1971; Mathias, 1971; Paine, 1971; Miller & Mann, 1973; Kofoed, 1975) and much attention has been paid to respiration of consumers in connexion with energy flow of whole communities (Jansson & Wulff, 1977; Pamatmat, 1968, 1977; Hargrave, 1969; Banse et al., 1971).

It is necessary for the understanding of the Wadden Sea ecosystem to go beyond measurements of isolated components and to combine measurements of primary and secondary production in order to ascertain the interactions of different parameters. This is possible using the bell jar technique (Zeitzschel & Davies, 1978; Zeitzschel, 1981}. Measurements of community metabolism were conducted in the Swedish Baltic Sea (Jansson & Wulff, 1977; Jansson et al., 1982). Similar studies of community metabolism of intertidal areas of the American Atlantic coast reveal the different characteristics of these areas compared to the Wadden Sea of the North Sea. One of the first measurements of community metabolism was conducted at the American Pacific coast (Pamatmat, 1968). Energy flow, carbon and nutrient cycles have been studied in various marine ecosystems (Odum, 1961; Odum & Smalley, 1959; Odum & Heald, 1972, 1975; Nixon et al., 1976, 1980; Pilson et al., 1979; Pomeroy et al., 1983}.

Questions about energy flow and community metabolism in the Wadden Sea have been raised by de Wilde (1980) and Kuipers et al. (1981}. These authors focussed their attention on comparing the significance of macrofauna with that of microbenthos (bacteria, microfauna, meiofauna}. They postulated the dominance of microbenthos in processes of metabolic turnover. Even the high productivity of microbenthos was pro- posed to be a result of a high input of detritus. Thus, the Wadden Sea would depend to a high degree on the North Sea (De Jonge & Postma, 1974).

Impor tance of g raz ing food chain 275

The presen t s tudy is conce rned with the p r ima ry and seconda ry p roduc t ion of th ree communities typical for the W a d d e n Sea of the North Sea coast. C o m m u n i t y m e t a b o l i s m was measu red in 1980, and ene rgy f low is ca lcu la ted . This s tudy is the first a t t empt to quantify ene rgy flow and the re la t ion of p r imary p roduc t ion to s econda ry p roduc t ion in benthic communi t i es of the nor thern W a d d e n Sea. The fo l lowing ques t ion ar ises: Which trophic groups of macro fauna spec ies a re impor tan t to product ion , communi ty me tabo l - ism and ene rgy flow? The p a t h w a y of ene rgy con ta ined in food l e a d i n g from p r ima ry to secondary p roducers should be clar i f ied.

Est imates are b a s e d on m e a s u r e m e n t s of communi ty structure, p r imary and secondary product ion, resp i ra t ion of s ingle spec ies as we l l as on the total oxygen consumpt ion of the communi t i e s (bell jar exper iments) .

AREA, MATERIAL AND METHODS

T h e s t u d y a r e a

Figure 1 shows the loca t ion of the " K 6 n i g s h a f e n ' , s i tua ted on the i s land of Sylt in the nor thern W a d d e n Sea (North Sea). The a rea of inves t iga t ion is e spec i a l l y su i tab le because of l i t t le domest ic , and no d i rec t indus t r ia l s e w a g e inf luence , also by the occurrence of the typ ica l d o m i n a n t in te r t ida l ben th i c communi t i e s of the W a d d e n Sea wi th in a small , we l l de f ined area. The spec ies compos i t ion of the microf lora communi t ies is s imi lar to that found in other a reas of the W a d d e n Sea (Brockmann, 1950; Col i jn & Koeman, 1975; Col i jn & Di jkema, 1981). The s t ructure of the mac ro fauna

Fig. 1. The "K6nigshafen" area (K) situated at the northern part of the island of Sylt (S) in the northern Wadden Sea (North Sea)


HW

50

NZO

-50

-100 LW

6xlOcmZsubsamples sorting without sieving sieved through 500/u m

sieved through 1000~u m

Fig. 2. Diagram of the important components of the communities Arenicola-flat, seagrass-bed, Nereis-Corophium-belt. The surfaces of the sediment cores mark the positions in cm in relation to midwater level (NZ). 1: bacteria, 2: microphytobenthos, 3: micro- and meiofauna, 4: Hydrobia ulvae, 5: Arenicola marina, 6: Macoma balthica, 7: Cerastoderma edule, 8: Scoloplos armiger, 9: Eteone long& 10: Littorina saxatilis, 11: Nereis diversicolor, 12: Tubificidae, 13: Corophium

voIutator, 14: larvae of diptera, 15: Zostera noltii, 16: epiphytic diatoms

communi t i es shows a pat tern which is essent ia l ly the same for sandflat areas of the ent i re W a d d e n Sea (Linke, 1939; Beukema, 1976). The "K6nigshafen" is roughly 4 km

long and 1 km wide. The tidal flats of the b ight are dra ined through a central tidal

channel . To the west and north, the bay is bordered by dunes separa t ing the area from

the open sea. To the south, marshy areas border the bay; at low tide 88 % of the total

"K6nigshafen" area are exposed. 55 % of the "K6nigshafen" area are inunda ted for less than 6 h. The t idal range has increased from 1.70 m to 1.80 m during the last few years.

The sed iments of the t idal fiats consist main ly of coarse sand; only in the western

part of the bay and b e t w e e n mussel beds are there larger areas of muddy sediments. Structures of macrofauna communi t i es of the "K6nigshafen" have been inves t iga ted

since 1937 (Wohlenberg, 1937). Woh lenbe rg def ined the different types of macrofauna communi t ies in the "K6nigshafen" . Reise (1978) descr ibed the communi t ies again,

showing a s imilar macrofauna distribution. In this s tudy the Arenicola marina (old)-

Scoloplos communi ty (Wohlenberg, 1937) includes the two sand flat communit ies . Areas of the sand flat communi t i es covered by seagrass, mainly Zostera noltii Hornem. and

lit t le Zostera marina L. are ca l led seagrass -beds in this study, and areas without seagrass

are def ined as Arenicola-flats. The sand flats just be low the h igh water mark are def ined as the Nereis-Corophium-belt . This a rea shows no se t t l ement of A, marina. During the inves t iga t ion Corophium volutator was scarce, but it has been very abundant in other

Importance of grazing food chain 277

years (Reise, 1978). The exper imenta l sites are s i tuated at different levels wi th different inundat ion times (Fig. 2). The Arenicola-flat extends from 0.75 m be low the midwater level to 0.10 m above midwater level. The exper imenta l site in this communi ty is situated at a level of 0.30 m below midwater level. The Arenicola-flat is i n u n d a t e d for 6 h dur ing one tide. The seagrass-bed covers the area b e t w e e n 0.10 m above midwater level and 0.40 m above midwater level. The exper imenta l site is located 0.20 m above midwater level. This site is i nunda t ed for 4 h dur ing one tide. Between 0.50 m above midwater level and the high water mark (0.70 m above midwater level) the Nereis- Corophium-belt forms a narrow belt. This site is i n u n d a t e d for only two hours.

C o m m u n i t y m e t a b o l i s m

The methods of field and laboratory measurement s employed in this study are expla ined in a d iagram (Fig. 3). Field measurement s of communi ty product ion and communi ty respirat ion were carried out every month us ing closed chambers (bell jars) dur ing submers ion time. Measurements of communi ty metabol i sm were not possible when the flats were covered with ice or on days with h igh w ind (above Beaufort 7). These bell jar exper iments were des igned to measure pr imary product ion and total respirat ion s imul taneously , Light bel l jars were ut i l ized to measure the pr imary production of the community, The total oxygen consumpt ion was measu red in dark bell jars. Small bel l jars ex tend 13 cm and larger bel l jars ex tend down to 30 cm deep into the sediment, 02 content in the bel l jars was de te rmined with the Wink le r - t echn ique every hour. The biological oxygen consumpt ion was calcula ted as the difference b e t w e e n total

FIELD WORK Ilight intensity I I

I be,,

1 1 F °mm ° ty

J benthic chamber J l--~primary I botLEp.L~ I I lproductivity 1

primary productivity Iprirnary productivity of microphytobenthos of phytop ankton

LABORATORY WORK

species composition,] biomass of plants J Jflo~

[temp eraturej I I

Idar bell jor I

I community respiration

iF pelagic J, respirationJ

small dark L J benth!c chamber I

J respiration of microbenthos J

I species composition, biomass, secondary production of macrofauna

f, respiration of J macrotauna j

chemicat oxygen demand of sediments

Fig. 3. Diagram of field and laboratory measurements


o x y g e n consumpt ion a n d chemica l oxygen demand . The chemica l oxygen d e m a n d was m e a s u r e d in smal l c h a m b e r s con ta in ing sed iments , wh ich were po i soned wi th formaldehyde . At the b e g i n n i n g and the end of each f ie ld e x p e r i m e n t run, nut r ien t samples (NO~, NO~, NH +, Si(OH)4) we re t a k e n from ins ide and outs ide the be l l jar. Results of nu t r ien t ana lys i s a re p r e s e n t e d in A s m u s (1984).

P r i m a r y a n d s e c o n d a r y p r o d u c t i o n

Every fortnight, p h y t o p l a n k t o n p roduc t ion was m e a s u r e d wi th two l ight and one da rk bot t le (300 ml} i n c u b a t e d in situ from 9 a.m. to 3 p.m. when h igh t ide was at noon. Mic rophy toben th i c p r imary p roduc t ion was m e a s u r e d wi th two l ight and one dark p l ex ig l a s chamber . Each c h a m b e r con ta ined a macrofauna- f ree s ed imen t l ayer of 0.3 cm th ickness . O x y g e n changes in the da rk chamber s r ep resen t the resp i ra t ion of bacter ia , microfauna, microflora, and chemica l Ou demand . The chambers were f i l led with f i l t rated, oxygen sa tu ra t ed sea wa te r and i n c u b a t e d in situ. Fur ther me a su re me n t s were car r ied out in the labora tory . For l abora to ry m e a s u r e m e n t s of macrofauna respirat ion, open f low- th rough m e a s u r i n g devices were ava i l ab le . Recordings were car r ied out over 6 h, the app rox ima te t ime of submers ion , and at in situ t empera tures . Phytoplankton s amp le s were t a k e n for cel l counts wi th an inver t ed microscope. Samples of microphytoben thos (core sampler : 0.64 cm 2 x 0.3 cm) were t aken dur ing the f ie ld measurements . Dia tom frustules from three s amp le s were c l e an e d and e m b e d d e d in Hyrax mount ing med ium. A fourth s a m p l e was p r e se rved wi th fo rma lde hyde to count those spec ies des t royed b y the c l e a n i n g procedure . Ca lcu la t ions of phy top l ank ton and microphytobenthos b iomass e x p r e s s e d in carbon uni ts were b a s e d on p l a s m a volume fol lowing the r e c o m m e n d a t i o n s of Edle r (1979).

The macro fauna of the cores, i n c l u d e d in the be l l jar, was sorted, a n d b iomass was de t e rmined . Sor ted m a t e r i a l was d r i e d at 75-100°C for th ree days. Ash we igh t was d e t e r m i n e d af ter combus t ion in a furnace at 600 °C for 2 h. Al l da t a of we igh t and b iomass are g iven in ash free dry weight . For p roduc t ion measuremen t s , the ind iv idua l s of d o m i n a n t spec ies we re s e p a r a t e d into yea r and w e i g h t classes. The month ly produc- t ion pe r m -2 was e s t ima ted from changes in m e a n i nd iv idua l we igh t and m e a n numer i - cal dens i ty of a w e i g h t c lass for e ach month us ing the fo l lowing equa t ion (after Winberg , 1971):

P = ( W 2 - Wl) x 1/2 (~1 + H2)

P is mon th ly product ion , W 1 and W 2 are m e a n i nd iv idua l we igh t s at t ime 1 and 2, and ~1 and B2 a re the m e a n numer i ca l dens i t i es at t ime 1 and 2.

RESULTS

S e a s o n a l c h a n g e s of p l a n t a n d a n i m a l b i o m a s s

In the flats inves t iga ted , the l iv ing o rgan ic subs tance at the s ed imen t surface is d o m i n a t e d by the b iomass of macrofauna . Biomass of mic rophy toben thos is smal l c o m p a r e d to this (Fig. 4). In the Arenicola-flat, ben th ic d ia toms are the bas is for p r imary p roduc t ion th roughout the year. M a x i m u m b iomass of ben th ic d ia toms is a l r eady r eached at the end of February . Phy top lank ton cont r ibu tes to the b iomass of p lants

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dur ing sp r ing and la te s u m m e r b looms (Asmus, 1982). The b iomass of macrofauna amounts to an annua l ave r age of 27.55 g afdw m -2 (Table 1). The g rea te r part of b iomass is con t r ibu ted by Hydrobia ulvae and Arenicola marina. The structure of b iomass and spec ies compos i t ion of the communi ty at the Arenicola-flat has b e e n desc r ibed ea r l i e r (Asmus, H., 1982; Asmus, R., 1982). The synchrony of seasona l d e v e l o p m e n t of p lant b iomass and month ly s econda ry p roduc t ion at tracts a t ten t ion (Fig. 4a-f).

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In the seag ras s -bed , the smal l seagrass Zostera noltii and its ep iphy te s (Fig. 5) are the most impor tan t p r imary p roducers in add i t i on to mic rophy toben thos and phy top lank - ton. Zostera noltii grows from M a y unt i l November . In t h e m i d d l e of Sep tember , seagrass forms the most dense cover, wh ich soon after is g r azed on by bren t geese and wigeons . In July, the h ighes t n u m b e r of ep iphy t i c d ia toms per uni t seagrass is reached , whi le h ighes t total n u m b e r pe r square me te r is r e ached in S e p t e m b e r due to h ighes t subs t ra te biomass. In la te winter , ben th i c d ia toms form m a x i m u m b iomass in the s e a g r a s s - b e d as in the Arenicola-flat. The m a x i m u m b iomass in the s e a g r a s s - b e d is half as h igh as the m a x i m u m in the Arenicola-flat. In summer, the b iomass of ben th ic d ia toms in the s e a g r a s s - b e d is lower than that of ep iphy t i c dia toms. Blue g reen a l g a e and phy top lank- ton const i tu te only a smal l par t of the total p l an t b iomass .

Mac ro fauna b iomass amounts to 30 g a fdw m -2 annua l average . The dominan t par t is fo rmed by H. ulvae and A. marina (Table 1).

In the Nereis-Corophium-bel t the b iomass of p lan t s is d o m i n a t e d by benth ic dia toms. As in the other communi t ies , h ighes t va lues of b iomass are r eached in late winter . Fo l lowing a d e c r e a s e from Apr i l to June, the b iomass of ben th ic d ia toms inc reases a g a i n and stays at this leve l unt i l December , in contras t to that in other areas. This h ighe r stock of ben th i c d ia toms p r o b a b l y can deve lop as a resul t of lower dens i ty of

Impor tance of graz ing food chain 281

macrofauna. Biomass of macrofauna is only half the annua l m e a n of the other two communit ies; thus total f eed ing act ivi ty is r educed dur ing the w a r m season. The most f requent ly encoun te red macrofauna species are H, u l v a e and N e r e i s d i ver s i co lor .

Table 1. Annual mean biomass and constancy of species of macrofauna in the area of study. The constancy of a species corresponds to the number of samples in which this species is present as percentage of the total number of samples. (Total number of samples in the Arenicola-flat: 18,

seagrass-bed: 18, Nereis-Corophium-belt: 16)

Species Nereis- Seagrass- Arenicola- Corophium-belt bed flat

biomass (g afdw m-2a -1) (constancy %)

G a s t r o p o d a Hydrobia ulvae (Pennant) Littorina saxatilis (Olivi) L. littorea L L. obtusata L. Retusa obtusa (Montagu)

B i v a l v i a Cerastoderma edule L. iVlacoma balthica L. Mya arenaria L. Myt i lus edulis L,

N e m e r t i n i Amphiporus lactifloreus (Johnston) Lineus viridis (Fabr,) Johnston

P o l y c h a e t a Arenicola marina L, Anai t ides mucosa (Oersted) CapiteHa capitata (Fabr.) Eteone longa (Fabr,) Harmothoe sarsi (Klingenberg) Heteromastus fi l i formis (Clap.) Nereis diversicolor (O. F. Mfiller) Nephthys hombergi Savigny Pygospio e legans Claparede Scoloptos armiger (0. P. Mfiller)

O l i g o c h a e t a Tubi fex spec. Edukemius beneden i Udekem

C r u s t a c e a Bathyporeia sarsi (Sars) Idothea balthica (Pallas) Jaera albifrons Leach Carcinus maenas L. Corophium volutator (Pallas) Crangon crangon L.

I n s e c t a larvae of diptera

12.83 (100) 25.21 (100) 19.47 (100) 0,04 (13) 0,75 (78) 0.01 ( 6 ) 0.12 (17) 0.04 (17)

0.01 (6) 0.01 ( 6 )

0.89 88) 0.01 13)

0.01 13) 0.01 19) 0.11 81)

1.49 94)

0.02 (75)

0.94 (I00) 0.01 (25)

0.08 (38)

0.02 (44)

0.27 0.74 0.45 0.01

0.01 0.02

1,72 0.22 0.08 0.03

0.01 0.35

0.06 0.12

0.01 0.01 0.01 0.01

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0.24 (94)

0.01 (33) 0.17 (100)

0.02 ( 6 )

0.02 ( 6 )

282 H. A s m u s & R. A s m u s

M o n t h l y p r ima ry p roduc t iv i ty

Values of primary productivity of the Arenicola-flat have already been described (Asmus, R., 1982). The course of monthly primary productivity is shown in Figure 6a+b. Primary productivity is highest in the seagrass-bed due to the productivity of Zostera noltii and its epiphytes, which only here adds to the productivity of microphytobenthos and phytoplankton. In the seagrass-bed, primary productivity of microphytobenthos is a little lower than in the Arenicola-flat (Fig. 6b). Maximum primary productivity starts

mgC,m'2d -~

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Fig. 6. Gross primary productivity a: of phytoplankton (Arenicola-flat: straight line, seagrass-bed: dotted line); b: of microphytobenthos (Arenicola-flat: straight line, seagrass-bed: dotted line); c: of microphytobenthos in the Nereis-Corophium-belt; d: gross and net (dotted line) primary productiv-

ity of Zostera noltii with epiphytes

I m p o r t a n c e of g r a z i n g food c h a i n 283

Table 2. Correlation between gross primary productivity and temperature or light intensity

Area Gross primary productivity and temperature

(ml O2m-2h-I/T°C)

Gross primary productivity and light

(ml O2m-2h-1/J m-2day -1)

A r e n i c o l a - f l a t community y = 1,35+ 5.74× y = - 5 1 3 . 6 6 + 37,88(lnx) productivity r = 0.91 n = 9 r = 0.91 n = 9 microphytobenthos y -- 6.19+ 2.66x y -- - 2 2 6 . 8 3 + 17.13(lnx) productivity r = 0.84 n = 14 r = 0.87 n = 15

S e a g r a s s - b e d community y - - 6.06+ 3,12x y = - 2 0 7 . 5 8 + I6.34(lnx) productivity r = 0.77 n = 9 r = 0.84 n = 9 (phytoplankton + microphytobenthos + Zostera noltii [per 1 g dry weight]) microphytobenthos y = 2.42+ 2.55 × y = - 173.25+ 13.50(lnx) productivity r = 0.70 n = 15 r = 0.77 n = 16

N e r e i s - C o r o p h i u m - b e l t microphytobenthos y = 19.27+ 2.52 x y = -- 137.82 + 12.46{lnx) productivity r = 0,57 n = 13 r = 0.67 n = 14

ea r l i e r in t he s e a g r a s s - b e d t h a n in t he Arenicola-flat. A d d i t i o n a l d i f f e r e n c e s a re l o w e r v a l u e s of p r i m a r y p r o d u c t i v i t y in t he s e a g r a s s - b e d in J u n e a n d S e p t e m b e r . P r ima ry

p ro duc t i v i t y of p h y t o p l a n k t o n is l o w e r t h a n on t h e Arenicola-flat d u e to t h e sho r t e r i n u n d a t i o n p e r i o d a n d l o w e r w a t e r c o l u m n (Fig. 6a). T h e ac t iv i ty of b e n t h i c d i a t o m s

d e t e r m i n e s the p r i m a r y p r o d u c t i v i t y in t he Nereis-Corophium-belt (Fig. 6c). P r ima ry

p roduc t iv i t y of m i c r o p h y t o b e n t h o s is h i g h e r t h a n in t he o the r two c o m m u n i t i e s bu t it

f luc tua tes s t rongly , e s p e c i a l l y in s p r i n g a n d s u m m e r . P r ima ry p r o d u c t i v i t y d e c r e a s e s f rom A u g u s t to D e c e m b e r . I n c r e a s i n g b i o m a s s of m i c r o p h y t o b e n t h o s is r e l a t e d to r i s ing

p r i m a r y p roduc t iv i ty . In con t ras t to this, t h e s tock of b i o m a s s of m i c r o p h y t o b e n t h o s d o e s not i n c r e a s e in the Arenicola-flat a n d in t he s e a g r a s s - b e d d e s p i t e i n c r e a s i n g p r i m a r y

p roduc t iv i ty . Here , h i g h p r i m a r y p r o d u c t i v i t y is m e a s u r e d in s u m m e r w h e n b i o m a s s of m i c r o p h y -

t oben thos is low. P r imary p r o d u c t i v i t y m e a s u r e d in b e l l jars a n d sma l l b e n t h i c c h a m b e r s

(mic rophy toben thos ) is s t rong ly c o r r e l a t e d w i t h t e m p e r a t u r e a n d l i gh t i n t e n s i t y in al l

t h r ee c o m m u n i t i e s (Tab le 2).

M o n t h l y s e c o n d a r y p r o d u c t i o n

In the Arenicola-flat, to ta l p r o d u c t i o n of m a c r o f a u n a a m o u n t s to 50 g a f d w m -2 a -1.

M a c r o f a u n a cons is t s for t he g r e a t e s t pa r t of Hydrobia ulvae, Arenicola marina, Macoma balthica and Scoloplos armiger (Asmus, 1982). T h e m a x i m u m tota l m a c r o f a u n a p r o d u c - t ion is r e a c h e d in sp r ing b e t w e e n Apr i l a n d May . N e a r l y ha l f t he a n n u a l p r o d u c t i o n has

b e e n f o r m e d by May. N e g a t i v e v a l u e s of p r o d u c t i o n a p p e a r in w i n t e r b e t w e e n the e n d of

F e b r u a r y a n d the e n d of March . In m i d s u m m e r ( J u l y / A u g u s t ) p r o d u c t i o n of m a c r o f a u n a

is low; it r i ses a g a i n t owards a u t u m n (Fig. 4d).


In the seagrass-bed, macrofauna produces 48 g afdw m -2 a - 1 Biomass amounts to 30 g afdw m -2 a -1 on average, from which follows a P/B-ratio of 1.60. H. ulvae has the greatest share in production, followed by A. marina and Littorina saxatilis. Seasonal variation of these shares is small. The maximum total macrofauna production is built up between March and April (Fig. 4e). During this time, one third of the annual production is formed. In summer, production decreases slowly down to the minimum in June. In midsummer, production of biomass rises again. From August till October, production values of the seagrass-bed are similar to those in the Arenicola-flat.

In the Nereis-Corophium-belt, total secondary production amounts to 17 g afdw m -2 a -1. Between May and June, maximum macrofauna production is reached, corres- ponding to a quarter of annual production (Fig. 4f). In spring (by June), half of the annual production has a l ready been formed. Production decreases in summer until a minimum is reached in autumn and winter.

A n n u a l b a l a n c e of p r i m a r y p r o d u c t i v i t y

Table 3a shows the parti t ioning of community primary productivity. The primary productivity of microphytobenthos is highest in the shallow Nereis-Corophium-belt, followed by lower production values in the Arenicola-flat and in the seagrass-bed. Net production means gross production minus respirat ion of total microbenthos in this connection. Supposing that the epiphytic diatoms of the seagrass produce per unit biomass (carbon) as much as the benthic diatoms in the seagrass-bed, the epiphytic annual mean productivity is est imated at 39.87 % _+ 16.37 (standard deviation) of the gross productivity of Zostera noltii. While pr imary productivity of phytoplankton is significant in the Arenicola-flat, planktonic productivity is two thirds less in the seagrass-bed; this results from a lower water depth and a shorter inundation period.

Primary productivity of the community is highest in the seagrass-bed. In the Arenicola-flat and in the Nereis-Corophium-belt, gross community primary productivity values are similar, al though microphytobenthos and phytoplankton contribute to the community production in the Arenicola-flat and only microphytobenthos is active in the Nereis-Corophium-belt. The P/R-ratio (quotient of gross primary productivity and total community respiration) is lowest in the Arenicola-flat and rises towards the seagrass-bed and the Nereis-Corophium-belt (Table 3c).

The difference between gross primary productivity and the total respiration can be calculated for the total area of the three communities. It reveals that the primary productivity of the large Arenicola-flat is most important (Table 3d).

A n n u a l b a l a n c e of s e c o n d a r y p r o d u c t i o n

The annual production of macrofauna is similar in the Arenicola-flat and in the seagrass-bed (Table 3b). Only about one third of this production is contributed by the Nereis- Corophium-belt.

The main part of production falls on Hydrobia ulvae. In the seagrass-bed and the Nereis-Corophium-belt, production of H. ulvae constitutes great fractions of 85 % and 80 %, while in the Arenicola-flat this percentage is lower (43 %). In the Arenicola-flat, the production of the lugworm Arenicola marina forms an important part of the annual

I m p o r t a n c e of g r a z i n g food c h a i n

Table 3a. Annual balance of primary productivity (gC m-2a -1)

285

Arenicola-flat Seagrass-bed Nereis-Corophium-belt

Microphytobenthos Gross Net

Phytoplankton Gross Net

Zostera noltii With epiphytes Gross Net

115 85 152 99 67 120

32 9 28 8

378 167

Table 3b. Annual secondary production


g afdw m -2 50.21 48.22 17.48 gC m -2 29.54 28,36 I0.28

Table 3c, Annual balance of the three communities


Gross primary 321 102m-2a -1 1034 102m-2a -1 332 102m-2a -1 productivity = 148 gC = 473 gC = 152 gC

Total respiration 179 102m-2a -1 540 102m-2a -1 130 102m-2a -1

Net primary 142 102m-2a -1 494 102m-2a -1 202 102m-2a -1 productivity = 65 gC = 226 gC = 92 gC

P/R 1.79 1.91 2.55

Table 3d. Primary productivity of the total area of the communit ies

Community Area Gross primary (ha) productivity

(to C)

Net primary productivity

considering total respiration (to C)

Arenicola-flat 121.61 179 79 Seagrass-bed 20.02 95 45 Nereis- Corophium-belt 21.80 33 20


p roduc t ion (30 %). Other spec ies p l a y a minor role in s econda ry product ion. In the Nereis-Corophium-belt, Nereis diversicolor has a p e r c e n t a g e of 9 % in annua l produc- t ion of the communi ty .

As the g raze r H. ulvae is dominan t in the three communi t ies , macrofauna gains the major par t of its e n e r g y for p roduc t ion via the g raz ing food chain. As ep iphy tes add i t i ona l l y are p re sen t in the s eag ra s s -bed , e n e r g y t ransfer th rough the g raz ing food cha in is of g rea te r impor t ance in this communi ty . In this communi ty , 83 % of ene rgy used for p roduc t ion are o b t a i n e d from the g raz ing food chain. In the Arenicola-flat and in the Nereis-Corophium-belt, the s ign i f icance of spec ies o ther than grazers is grea ter than in the seag ras s -bed .

C o m m u n i t y r e s p i r a t i o n

The es t ima tes of communi ty me t abo l i sm are b a s e d on m e a s u r e m e n t s of total oxygen consumpt ion and the i r annua l var ia t ions c o m b i n e d wi th f ie ld me a su re me n t s of b io logi - cal s e d i m e n t act ivi ty. The total oxygen consumpt ion ST is the sum of al l chemica l and b io log ica l oxygen consuming processes which inf luence the s ed imen t surface:

ST = SB + Sc

Oxygen consumption due to biological processes S B corresponds to the community

respiration in the oxic part of the environment. In this study, S B was calculated after subtraction of chemical oxygen consumption S c from total oxygen consumption S T. S c

was measured in formaldehyde poisoned sediments. In situ oxygen consumption of

microbenthos Smicro (including microfauna, microflora and bacteria) is the difference between oxygen demand of the sediment S A and chemical oxygen consumption of the

sediment S c. The difference between S T and S A is equal to in situ oxygen consumption of macrofauna. Respiration of single macrofauna species is determined with laboratory

experiments.

Total oxygen consumption

In the Arenicola-flat as well as in the seagrass-bed, total oxygen consumption inc reases from low va lues in win te r to a m a x i m u m in summer {Fig. 7). M a x imum total oxygen consumpt ion in the Arenicola-flat is a l r e a dy r eached in Ju ly whereas in the s e a g r a s s - b e d it r ises unt i l Sep tember , In contras t to that, in the Nereis-Corophium-belt total oxygen consumpt ion r ises in sp r ing to a h igh level . M a x i m u m oxygen consumpt ion is h ighes t in the s e a g r a s s - b e d (197 ml 02 m -2 h - l ) , fo l lowed by the Nereis-Corophium- be l t (136 ml 02 m -2 h - i ) . In the Arenicola-flat m a x i m u m oxygen consumpt ion is lower (52 ml 02 m -2 h - l ) . In the Arenicola-flat total oxygen consumpt ion r ises wi th increas ing t empera tu re . In the other communi t i e s the effects of t e m p e r a t u r e on total oxygen consumpt ion are s u p e r i m p o s e d by biot ic factors.

O x y g e n c o n s u m p t i o n of m a c r o f a u n a - f r e e s e d i m e n t s (SA)

High s e d i m e n t ac t iv i t ies could be m e a s u r e d e spec ia l ly in spr ing and ear ly summer in the Nereis-Corophium-belt. SA was low in the Arenicola-flat and in the seagrass bed. In the Arenicola-flat, oxygen consumpt ion of s ed imen t s var ies from 1.22 to 7.07 ml 02 m -2 h -1. On ly in July, w h e n the t e m p e r a t u r e r ises to about 20°C, is h igh oxygen

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C h e m i c a l o x y g e n c o n s u m p t i o n (Sc)

The amount of oxygen consumed by chemica l p rocesses (Sc) is much lower than that u sed by other processes . A v e r a g e va lues a re p r e s e n t e d in Asmus, H. (1982). S c shows no s ign i f ican t d i f ferences b e t w e e n the e x p e r i m e n t a l sites, bu t d e p e n d s s t rongly on temperature. Because of the r e l a t ive ly s imple s t ructure of the inves t iga t ed communit ies , some componen t s wi th ha rd ly m e a s u r a b l e act iv i t ies were neg l ig ib le . Espec ia l ly the respi ra- t ion of p l ank ton l ies wi th in the marg in of error for the used be l l jar t echn ique (1 ml 02 m -2 h - l ) . Because of the l ack of mac rophy te s in the Nereis-Corophium-belt and in the Arenicola°flat, the d i f fe rence b e t w e e n ST and SA rep resen t s macro fauna respi ra t ion only.

E s t i m a t e s

From the f ie ld m e a s u r e m e n t s of S T, S A, Sc, oxygen consumpt ion of macro- and microben thos could be e s t ima ted by ca l cu la t ing the di f ference us ing the equat ions above.

M i c r o b e n t h o s r e s p i r a t i o n : Smicro = S A - S c. In spring, the Nereis- Corophium-belt is cha rac te r i zed by in tense mic roben th i c respira t ion. This reflects the h igh act ivi ty of mic rophy toben thos which tends to form dense pa tches at that t ime. In the Arenicola-flat, microben th ic resp i ra t ion r anges from 0.6 to 2.6 ml 02 m -2 h -1. Only in Ju ly do va lues up to 18 ml 02 m -2 h -1 appear . Mic roben th i c resp i ra t ion in the seagrass- b e d is on a v e r a g e s l igh t ly h ighe r (0.1-7.6 ml 02 m -2 h-l}.

R e s p i r a t i o n o f m a c r o b e n t h o s : Smacr o -- ST--S A. In situ resp i ra t ion of mac roben thos equa l s the d i f ference b e t w e e n total oxygen consumpt ion of the community and oxygen consumpt ion of macrofauna- f ree sed iments , if macrophytes are absen t and resp i ra t ion of wa te r is of minor impor t ance (Fig. 7). In the Arenicola-flat and in the Nereis-Corophium-belt macrofauna is the only componen t of macrobenthos , in the s e a g r a s s - b e d m a c r o p h y t o b e n t h o s is impor tant . Respi ra t ion of mac roben thos const i tutes the g rea tes t share in oxygen consumpt ion in a l l th ree communi t ies . In the Nereis- Corophium-belt only, does resp i ra t ion of mic rophy toben thos domina te in spring. Using l abora to ry exper iments , shares of resp i ra t ion are a t t r ibu tab le to s ingle macrofauna species . In the Arenicola-flat, 18.59 ml 02 m -2 h -1 are r e sp i red by macrofauna, 19.09 ml 02 m -2 h -~ in the s e a g r a s s - b e d and 16.58 ml 02 m -2 h -1 in the Nereis-Corophium-belt. Macro fauna spec ies wi th h igh b iomass p r e d o m i n a t e the amoun t of respira t ion. Conse- quen t ly Hydrobia ulvae t akes the g rea tes t share in oxygen consumpt ion.

A n n u a l b a l a n c e of m a c r o f a u n a r e s p i r a t i o n

Al though macro fauna resp i ra t ion pe r hour is very s imi lar th roughout the year, macro fauna loses di f ferent quant i t i es of e n e r g y th rough resp i ra t ion (Arenicola-flat: 2237 k J, s eag ra s s -bed : 3280 k J, Nereis-Corophium-belt: 1425 k J); the dif ferences are a resul t of i nunda t ion t ime a n d thus of t i d e - i n d u c e d var ia t ions of macrofauna activity. Labora tory m e a s u r e m e n t s can d e t e r m i n e shares of the t rophic groups. Graz ing spec ies


cause the highest values of respirat ion accompl ished by det r i tus-feeding animals . Predators and suspens ion feeders are character ized by low overall oxygen consumption.

E n e r g y f low t h r o u g h t h e c o m m u n i t i e s

In the Arenicota-flat, plants ut i l ize 7257 kJ m -2 a -1 of solar energy for photosynthesis (gross pr imary productivity). Phytoplankton absorbs 18 % of this energy and microphytobenthos absorbs 82 %. Because of the structural complexi ty of the p lan t communi ty and the high biomass in the seagrass-bed, gross pr imary productivi ty is exceptional ly high (22914 kJ m -2 a- l ) . Seagrass uti l izes 4 1 % of this energy for gross primary productivity. Epiphytes produce further 38 %, and microphytobenthos has a share of 19 % in total gross pr imary product ivi ty in this community. The impor tance of phytoplankton is reduced drastically in the shal low area of the seagrass-bed (1.65 %). In the Nereis-Corophium-belt, only microphytobenthos is impor tant (7839 kJ m -2 a - l ) . Only a small part of the gross pr imary product ivi ty is stored as p lan t biomass. A large amount is respired and a still greater part is t ransported to h igher levels of the food web. It is difficult to dis t inguish be tween the respirat ion of plants and the total microbenthos in field experiments. Net pr imary product ivi ty is g iven as a result of substract ion of p lan t and microbial respirat ion from gross pr imary productivity. Total respirat ion of p lants and microfauna amounts to 9 9 9 k j m - 2 a -1 in the Arenicola-flat, 11900kJ m - 2 a -1 in seagrass-bed and to 1660 kJ m -2 a -1 in the Nereis-Corophium-belt. In the Arenicola- flat, net pr imary productivi ty is 6258 kJ m -2 a -1. In the seagrass-bed, 11014 kJ and in the Nereis-Corophium-belt 6178 kJ m -2 a -1 are t ransported as net pr imary productivi ty to higher trophic levels (Fig. 8).

Energy flow through the macrofauna in the Arenicola-flat amounts to 69 gC m -2 a -L Between February and March a very low energy flow is measurable . In spring, energy flow rises due to increas ing activity of the organisms. In May, energy flow starts to decrease and unt i l July it remains at a level of 10 gC m -2 month -1. In m i dsumme r and autumn, unt i l the end of October, energy flow is reduced further. Two thirds of the total energy assimilated by macrofauna flow through Hydrobia ulvae. The part of energy flow used for product ion is 43 %, that of respirat ion is 57 %. These percentages f luctuate in the course of the year. In spring, product ion surpasses respiration, whi le in summer a nd au tumn respirat ion consti tutes the m a i n part of energy flow. On the assumpt ion that sources of food are used in proport ion to their availabil i ty, 49 gC m -2 a -1 are t aken up by the grazing food chain and 20 gC m -2 a -1 are t aken up by the detri tus food chain. Taking into considerat ion the total area of the Arenicola-flat (121.6 ha) 8.34 × 107 gC or 83 to C a -1 are assimilated by the communi ty as a whole.

Energy flow through the macrofauna of the seagrass-bed amounts to 85 g C m -2 a -1. As in the Arenicola-flat, energy flow is h ighest in spring. In summer, va lues are lower, but they rise aga in in late summer. H. ulvae contr ibutes 89.7 % to total assimilat ion. The share of product ion is 33 % and the share of respirat ion is 67 %. In spring, the share of production in energy flow is high. 72 gC m -2 a -1 are t aken up by the graz ing food cha in and only 13 gC m -2 a -1 by the detri tus food chain. Energy flow per m 2 is highest in the seagrass-bed, bu t as its area is relat ively smal l (20.02 ha), only 1.70 × t07 gC a -1 (17 to C a -1) are taken up by the seagrass communi ty .

In the Nereis-Corophium-belt, energy flow is 35 gC m -2 a -1. In contrast to the other

290 H. Asmus & R. A s m u s

two a reas m a x i m u m in tens i ty of the e n e r g y flow is not r eached before June /Ju ly . In winter , e n e r g y flow is ha rd ly measurab le . Abou t two thirds of ene rgy flow through mac ro fauna are a t t r i bu tab le to H. ulvae in the Nereis-Corophium-belt. The share of p roduc t ion in total a s s imi l a t ion is 30 %, the share of resp i ra t ion is 70 %. In the first half of the yea r the par t go ing into p roduc t ion is h igher . Neve r is the par t u sed for product ion

11604

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Impor tance of g raz ing food chain 291

C 1323.0

4-

1660.0 10720

4 I

3068.0

160

o j8

242.0

J i

r 0.8 1980

I I 137.0

J

262.0

Fig. 8. Simplified models of energy flow of the three communities, a: Arenicola-flat; b: seagrass- bed; c: Nereis-Corophium-belt. Figures with the symbols represent annual mean biomass (kJ m-2). Incoming solar radiation (kJ m -2 a -1, 400-700 nm wavelength) is shown on the left side. Figures by the arrows above the symbols indicate the energy flow; figures below the symbols in the right side reveal the production. Respiration of single components is specified in the lower row. The final value on the lower left hand side gives the total community respiration. All figures indicating energy flow, respiration and production are annual mean values (kJ m -2 a-1). Tissue of macrofauna species shows different energy content. In this figure, 1 g afdw equals 17.83 kJ (gastropods); 17.82-20.77 kJ (bivalves); 17.70 (nernertines); 16.35 (Arenicola); 20.33 (other polychaetes); 16.10

(crustaceans); 22.29 (insect larvae) (cf. Jansson & Wulff, I977; Pollack, 19791

higher than that used in respiration, 26 gC m -2 a -1 are t aken up by the graz ing food

chain and 5 gC m - 2 a -1 are taken up by the detr i tus food chain. In the Nereis- Corophium-belt, ene rgy flow through macrofauna is less in tense than in the other two

communit ies . The total area of the Nereis-Corophium-belt in the "K6nigshafen" is

21.8 ha; thus, bas ing our ca lcula t ion on these est imates, 0.76 × 107 gC (7.56 to C) are

taken up per year.

DISCUSSION

The three communi t ies inves t iga ted differ dist inctly wi th regard to the structure of their plant and animal components . In the b iomass of the Arenicola-flat macrofauna,

suspension feeders and detri tus feeders const i tute a g rea te r part than in the seagrass-

bed. In the Nereis-Corophium-belt compara t ive ly more inver tebra te predators can be

found. The three communi t i es have in common the p r e d o m i n a n c e of the small snai l


Hydrobia ulvae. The macrofauna biomass is in the same range in the Arenicola-flat and seagrass-bed, whereas in the Nereis-Corophium-belt the biomass amounts to one third only. Differences in inundation time mainly result in different periods of grazing.

P r imary p roduc t iv i ty

The primary productivity of microphytobenthos is as high as reported for other intertidal areas (Marshall et al., 1971; van Raalte et al., 1976; Cad~e, 1980). The close correlations between primary productivity and light and temperature are in agreement with Leach (1970), Admiraal (1977), Colijn & van Buurt (1975), Rasmussen et at. (1983), but were not found in in situ measurements by Colijn & de Jonge (1984). A comparison of the P/R ratios with those found in other areas reveal that the P/R ratios of the "K6nigsha- fen" area are high (Pamatmat, 1968; Jansson & Wulff, 1977; Propp et al., 1980; Pomeroy & Wiegert, 1981). A P/R ratio above 1 is typical for a system in a "young" stage (Odum, 1980). When succession proceeds or pollution increases the P/R ratio will decrease, as can be observed in the Ems-Dollard-estuary (van Es, 1982). In deeper water (20-25 m), on muddy sediments, respiration is higher than primary production, whereas on sand, photosynthesis may be appreciable at this depth (Propp et al., 1980). The primary productivity of Zostera noltii lies within the range of productivity measured in other areas (120-320 gC m -2 a- l ; Mann, 1982), with the exception of an investigation in the Lake Grevelingen (Lindeboom & de Bree, 1982) where an extremely low value of 20 gC m -2 per growing season net productivity was found.

Compared with the scale of primary productivity in different areas of the oceans (Ryther, 1969), the primary productivity in the Arenicola-flat and in the Nereis- Corophium-belt is in the upper range of the productivity on the continental shelf. The primary productivity in the seagrass-bed is in the range of very high productive areas. The primary productivity of the whole sand flat is to be considered as high, but not as extremely high. The importance of the different groups of primary producers may vary distinctly even in other shallow waters. In the Wadden Sea, microphytobenthos is the most productive group, whereas in tropical lagoons phytoplankton and mangrove trees are found to be more important than microphytobenthos and seagrass (Day et al., 1982). In several shallow water areas of the Baltic, the main part of primary production is stored in the biomass of macroalgae and therefore it is not available to herbivore grazing.

S e c o n d a r y p roduc t ion

The first estimate of secondary production of macrofauna was possible by using the Boysen-Jensen-method (Boysen-Jensen, 1919). Seasonal variations of total biomass of macrofauna were observed by Beukema (1974, 1981). Often secondary production of populations of single species is investigated, and the production of the whole community has to be calculated with the aid of data not measured simultaneously. In this study, secondary production is determined as the product of individual growth increments and mean population density. Because significant changes in biomass of populations do not occur during the year, it can be inferred that elimination of biomass is just compensated by secondary production. Secondary production in the "K6nigshafen" is comparable to that in other intertidal areas and estuaries (13 g afdw m -~ a- l ; Warwick & Price, 1975;


120 g afdw m -2 a -1 [maximum]; Wolff & de Wolf, 1977). Up to now, est imates of secondary product ion of macrofauna amoun t to 30 g afdw m -2 a -~ for the Dutch W a d d e n Sea, based on values of b iomass de t e rmined after s ieving with 1 mm mesh (Beukema, 1981). Production of organisms pass ing through a sieve of 1 mm mesh size is considered to be low (up to 10 g afdw m -2 a-~; Beukema, 1981). Secondary product ion of larger macrofauna is men t ioned to be 18 g C (Beukema, 1981), thus 18 % of pr imary product ion is used directly for secondary product ion of larger macrofauna.

If the product ion of Hydrobia ulvae (12.6 g C m -2 a -1) were d is regarded in this investigation, secondary product ion would amount to 17 g C m -2 a - I in the Arenicola- flat which is s imilar to sand flats of the Dutch W a d d e n Sea. Kuipers et al. (1981) have shown that food supply consis t ing of 100 g C m -2 a -1 pr imary product ion and 250 g C m -2 a -1 detritus input (de Jonge & Postma, 1974) is used up by secondary product ion (18 g C m -2 a -1) to only a low degree. The small food web which inc ludes microfauna and small macrofauna like H. ulvae fills this gap represen t ing a l ink b e t w e e n pr imary and secondary producers. From meiofauna biomass which consists ma in ly of nematodes , Witte & Zijlstra (1984) es t imated a secondary product ion of meiofauna of 3.6 g C m -2 a -1 at Balgzand. Together with a product ion of 12.6 g C m -2 a -1 for small macrofauna in our investigation, it leads to a value of 16.2 g C m -2 a -1 for secondary product ion of the small food web.

This value shows that the product ion of the small food web inc lud ing microfauna and small macrofauna can amount to a similar order of magn i tude as product ion of larger macrofauna.

C o m m u n i t y r e s p i r a t i o n

In a community, total a n n u a l oxygen consumpt ion of sed iment surface is a realist ic measure of that part of organic mater ia l respired in the sed iment (Hargrave, 1972; Pamatmat, 1975). Communi ty metabol i sm is underes t ima ted by measuremen t s of oxygen consumpt ion in a communi ty where anaerobic processes take place. Further difficul- ties in in terpre ta t ing results of bel l jar exper iments arise through differences b e t w e e n the oxygen budget of dis turbed and und i s tu rbed sediments . The ba lance of erosion and sedimenta t ion de termines to what degree energy flow of the communi ty can be calculated from oxygen demand (Pamatmat, 1975). Strong storms may reactivate mater ia l in sheltered shallow bays like the "K6nigshafen". Measurement s which are only possible on days of qui te calm weather give a realist ic picture of the ene rgy flow and aerobic communi ty metabolism.

Annua l oxygen demand amounts to 180 1 m -2 a -1 (Arenicola-flat), 540 1 m -2 a -1 {seagrass-bed) and 1301 m - 2 a -1 (Nereis-Corophium-belt). Respective differences be tween the amounts of total oxygen consumpt ion of the three communi t ies are consid- erable. Respiration is highest in the seagrass-bed as a result of the p redominan t respirat ion of Zostera noltii. Respiration amounts to 64 ml O z m -2 h -1 on average in the seagrass-bed. In the Arenicola-flat, communi ty respirat ion is p redomina ted by macrofauna. In the Nereis-Corophium-belt, the par t ic ipat ion of macrofauna in respirat ion varies strongly (9-68 %); in the seagrass-bed only 20 % of communi ty respirat ion are contr ibuted by macrofauna because of high seagrass respiration. Total amounts of macrofauna respirat ion at the three stations are very s imilar despi te their different shares in communi ty respiration.


Partit ioning of respiration of different shallow water communities revealed 45 % macrofauna respiration on average (Zeitzschel & Davies, 1978). In the Arenicola-flat the part icipation of macrofauna in respiration is quite high while in the other two areas it corresponds with data in l i terature (Banse et al., 1971; Pamatmat & Banse, 1969; Smith et al., 1972).

Sediments of the Arenicola-flat are characterized by large individuals of Arenicola marina. A high percentage of macrofauna respiration in total respiration can be due to the presence of large sized macrofauna individuals (Nichols, 1972). Pamatmat (1975) did not find this relationship and concluded an anaerobic metabolism of large individuals in in situ experiments, whereas rates of oxygen consumption were high in laboratory experiments at conditions of oxygen saturation. It is known that A. marina may shift to anaerobic metabolism (Sch6ttler, 1980). It is open to discussion whether oxygen defi- ciency occurs in the burrows of A. marina even when the water above is oversaturated (150-200 %) as in the "K6nigshafen" when the worm repeatedly pumps water through its burrow (Baumfalk, 1979). At low tide, mussels may have switched over to anaerobic metabolism.

Up to now there is no indication of anaerobic metabolism in the dominant species of the three communities, Hydrobia ulvae. In previous studies, macrofauna respiration may have been underes t imated because the bell jars may have been too small or may have caused the burrows to clog with sediment by disturbing the surrounding area.

The results of bell jar experiments in areas free of macrophytobenthos show oxygen demand of 1-190 ml 02 m -2 h -1 (Duff & Teal, 1965; Pomeroy, 1959, 1960; Teal & Kanwisher, 1961; Wieser & Kanwisher, 1961). Most values range from 15-50ml 02 m -2 h -1. Mean oxygen consumption of 23 ml 02 m -2 h -1 (Arenicola-flat) and 59 ml 02 m-2 h-1 (Nereis-Corophium-belt) are in agreement with this range. In the seagrass-bed, the value of community respirat ion is relat ively low compared with other macrophytobenthos communities. But Z. noltii grows actively only from June to October. During this period, the mean value of respiration is 109 ml 02 m -2 h -1 and corresponds to values from other phytal regions (Jansson & Wulff, 1977; Asmus et al., 1980). In the Dutch Wadden Sea, first measurements of community metabolism suggest that oxygen is mainly taken up by the small food web (bacteria, microfauna, small macrofauna), while maximum macrofauna respiration should only be 20-30 % (Kuipers et al., 1981). Van Es (1982) points out the important role of bacteria in community metabolism. However, the methods of measurements are so different (e.g. at low tide) that the results do not seem to be comparable. Microbenthic algae often dominate respiration of microbenthos (Wieser & Kanwisher, 1961; Pamatmat, 1968), while microfauna has a medium share of 10-30 % (Wieser & Kanwisher, 1961). In the area of investigation, respiration of microbenthos was high only at temperatures of about 20 °C, and probably caused by bacteria (Asmus, 1983). In winter, values of microbenthos respiration were general ly low, higher values found occasionally were due to algal activity. The role of microfauna is only of minor importance for the oxygen budget al though microfauna is very abundant in the area (see Reise, 1981 a, b). Nematodes and copepods predominate in the microfauna. In July 1980, an average of 875000 nematodes and 240000 copepods per square meter lived in the upper 5 cm of sediment in the Arenicola-flat (Reise, pers. communication). Assuming that respirat ion of nematodes is 1.5 ml 02 g-~ wet weight and that respiration of harpac- t icoides is 1.0 ml g-1 wet weight (Jansson & Wulff, 1977), total respiration of nematodes


and copepods amounts to 0.43 ml 02 m -2 h -1 and 0.30 ml m -2 h -1 respectively. Respira- tion of microfauna might not be higher than 1 ml 02 m -2 h -1 in the warmest month of the year. It is certainly lower during the colder seasons. Values of this magni tude are negligible compared with the importance of other components even if one supposes higher abundance due to microfauna living in burrows of macrofauna (Reise, 1981a).

E n e r g y f low

Solar radiation is the major energy source for the community investigated. Other sources of energy from outside seem to be of minor importance. Detritus input is assumed to be high in many other intertidal areas, which in most cases show high sedimentat ion rates during high tides. The sediments of the communities studied are characterized by coarse sands with a relatively low detritus content. Microscopical analysis shows that the detritus is produced by members of the community itself. This leads to the assumption that sedimentation of detritus material may be low in general. Only strong sediment reworking through storms causes an increase in detritus content and transport of the water for a short time. But these processes have not been quantified up to now. Energy from solar radiation is incorporated into plants. Primary production of microphytobenthos does not cause an increase in plant biomass. A storage of energy does not occur. Production is used to compensate biomass losses through feeding by heterotrophs. A high abundance of herbivorous macrofauna decreased biomass and production of benthic microalgae in other areas (Hargrave, 1970; Darley et al., 1981; Pace et al., 1979; Davis & Lee, 1983; Hickman & Round, 1970; Taasen & Heisaeter, 1981; Branch & Branch, 1980; Connor et al., 1982), whereas a lower densi ty of macrofauna may stimulate the growth of microphytobenthos (Hargrave, 1970; Connor et al., 1982), In the Nereis- Corophium-belt, biomass losses of microphytobenthos caused by herbivores amount to only one third to one half the losses in other communities. Thus, a higher level of microphytobenthos biomass can be maintained.

Macrophytes and epiphytes grow only from May until November, and only from August to September does the macrophytic and epiphytic biomass exceed the biomass of the other compartments. In the other half of the year, no biomass of Zostera and epiphytes is developed; thus mean annual biomass of this compartment is relat ively low. Zostera loses a significant part of the assimilated energy by its own respiration and a minor amount of energy remains for production of biomass. This production leads to an increase in biomass and forms an energy storage during the vegetat ion period. At the end of the vegetation period, most of the energy stored by Zostera plants is lost to herbivorous birds. In most of macrophytobenthos based systems the plant biomass is utilized for higher trophic levels only after degradat ion to detritus (Mann, 1982). After defoliation in autumn, waves and tidal currents wash the leaves of Zostera noltii onto the shore, where degradat ion processes take place, and only a part of seagrass production will enter the detritus pool of the seagrass bed. Interactions be tween primary and secondary producers are so intense that the question arises whether pr imary production per year is high enough to maintain the macrofauna community. In the three communities investigated, primary production is usually higher than secondary production.

In the Arenicola-flat, 68 % of secondary production are uti l ized by the grazing food chain. This share is highest in the seagrass-bed (83 %), while in the Nereis-Corophium-


belt it is 76 %. The total amount of primary production is reflected in the degree of utilization by the grazing food chain. Values of primary production and secondary production are shown in Table 4. Primary production of benthic diatoms is uti l ized in the Arenicola-flat and seagrass-bed with an efficiency of 20 % more effectively than in the Nereis-Corophium-belt, where efficiency is only 7 %.

Epiphytes are used with an efficiency of only 7 %. This low efficiency is caused by the low biomass of consumers at the beginning of summer. Numbers of consumers increase during the next season.

Even secondary production is lower in summer than at the beginning of the year. Due to higher temperatures in summer, more energy has to be spent for respiration, thus epiphytic primary production is converted into macrofauna secondary production to a much lower extent. The efficiency of energy transfer from total primary production (without macrophytes) to total secondary production is 29 % (Arenicola-flat), 14 % (seagrass-bed) and 9 % (Nereis-Corophium-belt). It shows that primary production of all three communities is sufficient to meet the food demand of the macrofauna communities. A further increase of production efficiency is impossible, because food supply is spent to a high degree for macrofauna respiration especial ly in summer.

Secondary production forms the main source of food for invertebrate and vertebrate predators on the t idal flat. In this investigation only small predators could be considered (Anaitides, Nereis, Lineus etc.) which are permanent ly present on the tidal flat. These predators use only a small part of the biomass built up by secondary producers. The main part of secondary production is consumed by larger predators visiting the tidal flat during high tide, or by predat ing birds during low tide. Secondary producers are strongly affected by predators (Reise, 1978), but the knowledge about the energy transfer from this trophic level to the tertiary producers is still insufficient. About 260-816 kJ m -2 a -1 are avai lable to tertiary producers according to the estimates of this study.

I m p o r t a n c e of g r a z i n g food c h a i n

Effects of grazers upon primary producers could be observed in the three communities studied. These interactions affect the stock and production of different trophic levels as well as the structure of trophic elements in the communities. The great importance of benthic diatoms as food source is reflected in the production and biomass of herbivorous macrofauna. Due to the dominance of Hydrobia ulvae in the three communities the main pathway of energy can be described as beginning with benthic diatoms leading chiefly to small grazing animals and to higher trophic levels.

The following arguments support the great importance of the grazing food chain: (1) Autochthonous primary productivity is sufficient to meet the food requirements of macrofauna. (2) Macrofauna of the communities invest igated is dominated by species which feed on primary producers. The dominant H. ulvaeprefers benthic diatoms as food (Fenchel & Kofoed, 1976; Jensen & Siegismund, 1980). (3)In spite of high primary productivity during summer, the biomass of benthic primary producers does not accumu- late.

Hence, the community does not need an import of detritus from outside to maintain its high macrofauna biomass. There is no evidence that benthic microalgae are rejected as food in favour of detrital particles.


Are t h e s e r e s u l t s r e p r e s e n t a t i v e for o t h e r y e a r s a n d o t h e r i n t e r t i d a l a r e a s ? D u r i n g

th i s i n v e s t i g a t i o n t h e c l i m a t i c c o n d i t i o n s w e r e b y n o m e a n s u n u s u a l . S u m m e r t e m p e r a -

tu res c o i n c i d e d w i t h t h e l o n g t e r m a v e r a g e of t h i s a r e a , w h e r e a s t h e m e a n w i n t e r

t e m p e r a t u r e s 1979 /80 w e r e s l i g h t l y l o w e r t h a n t h e l o n g t e r m a v e r a g e .

B e n t h i c d i a t o m s a r e k n o w n as i m p o r t a n t p r i m a r y p r o d u c e r s i n m o s t i n t e r t i d a l a r e a s

a n d t h e y b u i l d u p a r i c h food s o u r c e for g r a z i n g a n i m a l s , b u t t h e i r r o l e for m a r i n e food

w e b s h a s b e e n u n d e r e s t i m a t e d in t h e pas t . A l t h o u g h s e d i m e n t s in K b n i g s h a f e n a r e

r e l a t i v e l y c o a r s e g r a i n e d , t h e m a c r o f a u n a c l o s e l y r e s e m b l e s t h o s e of o t h e r t i d a l a r e a s i n

n o r t h w e s t e r n E u r o p e (see W o h l e n b e r g , 1937), a n d t h e s p e c i e s c o m p o s i t i o n i n t h e t i d a l

z o n e h a s r e m a i n e d r e l a t i v e l y s t a b l e o v e r t h e l a s t d e c a d e s (Reise, 1982). F r o m t h e s e a r e a s

a n d a l so f rom o t h e r t i d a l f l a t s i n t h e w o r l d , h i g h a b u n d a n c e s of g r a z e r s a r e w e l l k n o w n

( M a c n a e & Kalk , 1962; DSrjes , 1978; P a c e e t al., 1979; B r a n c h & B r a n c h , 1980; Race ,

1982). C o n s e q u e n t l y , i t c a n b e e x p e c t e d t h a t t h e p a t t e r n of e n e r g y f l ow a n d t h e i m p o r t a n c e

of g r a z i n g food c h a i n of s i m i l a r i n t e r t i d a l s a n d b o t t o m s w i l l b e c o m p a r a b l e to t h o s e in

th i s s tudy , a n d t h a t t h e b e n t h i c g r a z i n g food c h a i n h a s a g r e a t e r i m p o r t a n c e t h a n

s u p p o s e d t i l l now.

Acknowledgements. The authors are indeb ted to the former director of the Biologische Anstal t Helgoland, Prof. Dr. O. Kinne, for the hospital i ty at the Littoral Station in List. Dr. K. Reise, Prof. Dr. H. Theede and Prof. Dr. B. Zeitzschel promoted this study with helpful advice. Thanks are due to Mrs. G. Kredel and Mrs. D. Barthel for kindly revis ing the Engl ish text, and also to the members of the Littoral Station. A grant was awarded by the Fr iedr ich-Naumann-St i f tung and by the Deutsche Forschungsgemeinschaft .

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