Download Benthic grazers and suspension feeders: Which one assumes the

HELGOLANDER MEERESUNTERSUCHUNGEN
Helgolfinder Meeresunters. 48,217-231 (1994)
Benthic grazers and s u s p e n s i o n feeders: w h i c h o n e
a s s u m e s the e n e r g e t i c d o m i n a n c e in KSnigshafen?
H. A s m u s
Biologische Anstalt Helgoland, Wattenmeerstation Sylt; D-25992 List,
Federal Republic of G e r m a n y
ABSTRACT: Size-frequency histograms of biomass, secondary production, respiration a n d energy
flow of 4 dominant macrobenthic communities of the intertidal bay of K6nlgshafen were analysed
and compared. In the shallow sandy fiats (Nereis-Corophium-belt [N.C.-belt], seagrass-bed and
Arenicola-flat) a bimodal size-frequency histogram of biomass, secondary production, respiration
and energy flow was found with a first peak formed by individuals within a size r a n g e of 0.10 to
0.32 m g ash free dry weight (AFDW). In this size range, the small prosobranch Hydrobia ulvae was
the dominant species, showing maximal biomass as well as secondary production, respiration and
energy flow in the seagrass-bed. The second peak of the size-frequency histogram was formed by
the polychaete Nereis diversicolor with individual weights of 10 to 18 m g AFDW in the N.C.-belt,
and by Arenicola marina with individual weights of 100 to 562 m g AFDW in both of the other sand
fats. Biomass, productivity, respiration a n d energy flow of these polychaetes increased from the
Nereis-Corophiurn-belt, to the seagrass-bed, and to the Arenicola-flat. Mussel b e d s surpassed all
other communities in biomass a n d the functional parameters mentioned above. Size-frequency
histograms of these parameters w e r e distinctly unimodal with a m a x i m u m at a n individual size of
562 to 1000 mg AFDW. This size group was dominated by adult specimens of Mytilus edulis.
Averaged over the total area, the size-frequency histogram of energy flow of all intertidal flats of
K6nigshafen showed one peak built by Hydrobia ulvae a n d a second one, mainly formed by A4.
edulis. Assuming that up to 10 % of the intertidal area is covered by mussel beds, the m a x i m u m of
the size-specific energy flow will b e formed by Mytilus. W h e n only 1 % is covered by mussel beds,
then the energy flow is dominated by H. ulvae. Both animals represent different trophic types a n d
their dominance in energy flow has consequences for the food web a n d the carbon flow of the total
area. If the energy flow of the macrozoobenthos of KSnigshafen is dominated by A4. edu//s, then the
primary energy has to be gained from the pelagic primary production a n d the total ecosystem will b e
d e p e n d e n t on energy input from the North Sea and deeper parts of the adjacent W a d d e n Sea. In the
case of a dominance of H. ulvae, the energy flow of K6nigshafen is mainly b a s e d on autochthonous
primary production.
INTRODUCTION
M a n y p a r a m e t e r s s t r u c t u r i n g f a u n a l a s s e m b l a g e s s h o w a d i s t i n c t size d i s t r i b u t i o n .
T h e r e l a t i o n b e t w e e n a b u n d a n c e a n d b o d y size h a s b e e n m o d e l l e d as a p o w e r f u n c t i o n .
From terrestrial populations, some authors have reported negative exponents (Brown &
M a u r e r , 1986; D a m u t h , 1987; 1991), w h i l e o t h e r s s h o w e x p o n e n t s n o t s i g n i f i c a n t l y
d i f f e r e n t f r o m z e r o ( M o r s e e t al., 1988). T h e f o r m e r i m p l i e s t h a t i n t h e s e p o p u l a t i o n s ,
s p e c i m e n s u s e e q u i v a l e n t a m o u n t s of e n e r g y r e g a r d l e s s of t h e i r b o d y size, w h i l e t h e
l a t t e r i m p l i e s a n e n e r g e t i c d o m i n a n c e b y l a r g e r i n d i v i d u a l s (Griffiths, 1992). T h e s l o p e of
9 Biologische Anstalt Helgoland, H a m b u r g
218
H. Asmus
a b u n d a n c e - s i z e relations m a y be a test of the hypothesis that e n e r g y a'vailability limits
the a b u n d a n c e of differently sized organisms. In n a t u r a l assemblages, this is only true for
d o m i n a n t species (Blackburn et a l , 1993). Since the e n e r g y supply is also s i z e - d e p e n dent, the size distribution has a major impact on respiration (Gerlach et al., 1985), growth
processes (Schwinghamer et al., 1986; Edgar, 1990 a; Barry & Tegner, 1990) and, as a
result, on the biomass of an a n i m a l a s s e m b l a g e (Heip et al., 1984; B o u d r e a u x & Dickie,
1992). Showing the s i z e - d e p e n d e n c e of these parameters, it will be possible to obtain
information on the effects of animal size within the food web. As a p a r a d i g m , predation is
strongly related to prey size and, if so, the e n e r g y flow from one trophic l e v e l to the next
be size-controlled (Cohen et al., 1993).
Structuring the metabolic a n d growth parameters of an a n i m a l a s s e m b l a g e in
relation to body size m a y lead to a w a y to predict the d y n a m i c role of a n i m a l a s s e m b l a g e s
on the ecosystem level. The importance of body size for productivity of m a r i n e f a u n a is
recognized by m a n y authors (Banse & Mosher, 1980; S c h w i n g h a m e r et al., 1986), m a i n l y
from a theoretical point of view. Recent investigations show the practical applicability of
m a k i n g use of the size structure for m e a s u r e m e n t s of secondary p r o d u c t i o n (Edgar,
1990a).
In the tidal flats of K6nigshafen, m a c r o f a u n a shows a wide r a n g e of sizes from small
ohgochaetes to large adult mussels a n d polychaetes. The question arises, w h e t h e r
d o m i n a n t macrofaunal assemblages show different size-frequency histograms of
metabolic a n d growth characteristics a n d what the reasons a n d c o n s e q u e n c e s are for the
entire ecosystem.
MATERIAL AND METHODS
S t u d y site
KSnigshafen is a small intertidal b a y (4 km2), situated at the n o r t h e r n tip of the island
of Sylt in the North Sea. Sand d u n e s form a small s a n d b a r which protects the b a y in the
north and the west from the open North Sea. To the east, the bay is o p e n to the W a d d e n
Sea. The tidal flats are drained by a central channel. The average tidal r a n g e is a b o u t
1.8 m, with only minor deviations due to n e a p a n d spring tides or s t r o n g winds. The
sediments are m a i n l y sandy with a distinct share of w i n d b o r n e sand from a d j a c e n t dunes.
M u d d y sediments are only found in a sheltered b a s i n in the west. For this investigation,
4 sites were selected which are a s s u m e d to be representative of the d o m i n a n t macrofaunal assemblages. The Nereis-Corophium-belt (N.-C.-belt) borders the m e a n high tide
line a n d is 20 to i00 m wide. It is i n u n d a t e d for n e a r l y 2 h during a tidal cycle. The u p p e r
part of the sand flat is covered by seagrass-beds which are i n u n d a t e d 4 - 5 h d u r i n g a tidal
cycle. O n s a n d y sites, the small seagrass Zostera noltii is dominant, w h e r e a s on m u d
Zostera marina is more a b u n d a n t . O n bare sandflats from the u p p e r shore d o w n to the
low-water hne, the lugworm Arenicola marina shapes the character of the sediment.
Because of the wide distribution of this a s s e m b l a g e over a wide r a n g e of tidal levels, a
study site at m e a n - t i d e level ( i n u n d a t i o n of 6 h per tidal cycle) w a s selected. This
Arenicola-flat has the greatest share in the total area of KSnigshafen. N e a r the low-tide
line, mussels form d e n s e beds. The areal coverage of mussel beds v a r i e d in the past
particularly d u e to ice scour d u r i n g severe winters a n d dredging by a n e x p a n d i n g mussel
fishery. The areal extension of the macrofaunal assemblages is shown in Table 1.
Benthic grazers a n d suspension feeders
219
Table I. Areal extension of macrofaunal assemblages of K6nigshafen in 106 m2, considering different
situations of areal coverage by mussel beds. Mud flats (0.3 to 0.4 x 106 m2) are not considered
Community
Nereis-Corophium-belt
Seagrass-bed
Arenicola-flat
Mussel bed
1%
10 %
0.34
0,31
3.03
0.05
0.34
0.46
2.45
0.48
Sampling procedure
Biomass data from macrofauna of the three sand flat communities were o b t a i n e d
during a n investigation of productivity a n d community metabolism in 1980. Two cores
(area: 600-700 cm 2) were e x a m i n e d every m o n t h in each of these assemblages i n order to
measure biomass a n d secondary production. A subsample of 10 x 10 cm surface area was
t a k e n from these cores a n d sieved through a 500-~m mesh sieve. This s u b s a m p l e was
used to analyse biomass a n d a b u n d a n c e of the smaller macrofauna, such as Hydrobia
ulvae, Pygospio elegans, juvenile polychaetes a n d ohgochaetes. The rest of the s e d i m e n t
was sieved through a 1000-~m sieve, to retain the larger macrofauna. Due to the greater
variabihty in the structure of habitat, 6 core samples (surface 10 x 10 cm) were t a k e n at
6 sites of the mussel b e d every m o n t h during the whole of 1984. The samples w e r e sieved
through 500-~m mesh. From these samples, the total m a c r o f a u n a was c o u n t e d at the
species level. W h e n animals occurred over a larger size range, different size classes were
counted separately.
D e t e r m i n a t i o n of b i o m a s s a n d s e c o n d a r y p r o d u c t i o n
The macrofaunal material was separated into species a n d size groups. These samples
were dried at 75 ~ for a b o u t 3 days. After cooling in a desiccator, the samples were
weighed. To d e t e r m i n e ash free dry weight (APDW), all samples were b u r n t in a furnace
at 550 ~ These data were used to estimate the individual weight as well as the biomass
per square metre of species a~d size groups.
Secondary production was estimated for each species a n d size group from c h a n g e s in
individual weight a n d from the m e a n a b u n d a n c e b e t w e e n two s u b s e q u e n t s a m p l i n g
dates (Crisp, t984; Asmus, 1987; Brey, 1990). These m o n t h l y estimates were extrapolated
to one square metre, a n d a d d e d up for a o n e - y e a r period for species a n d size classes
separately. S u m m i n g up yearly production values of all species of a c o m m o n size group
gave the secondary production of this size group. In order to compare biomass a n d
production values with carbon flow, l g AFDW was a s s u m e d to correspond to 0,58 g C
(derived from J a n n s s o n & Wulff, 1977; Remmert, 1980).
Respiration measurements
For the d o m i n a n t m a c r o f a u n a species, respiration m e a s u r e m e n t s were carried out in
closed chambers in the laboratory u n d e r in situ temperatures. From these m e a s u r e m e n t s
220
H. Asmus
a n allometric regression was calculated b e t w e e n respiration a n d i n d i v i d u a l w e i g h t for
each of the d o m i n a n t species (Asmus, 1984). Respiration rates of rare species were
estimated from the individual sizes, u s i n g the allometric regression of the d o m i n a n t
species most similar in taxonomic order a n d size. Respiration from these e x p e r i m e n t s was
a s s u m e d to reflect a m e a n routine m e t a b o l i s m of the species investigated. Hourly
respiration was converted to daily respiration considering the m e a n i n u n d a t i o n time of
the community. Respiration d u r i n g low tide was a s s u m e d to be negligible. Most of the
investigated species are inactive d u r i n g low tide, a n d m e e t their metabolic r e q u i r e m e n t s
b y anaerobiosis. This i n d u c e s a n oxygen debt which will b e c o m p e n s a t e d at the
b e g i n n i n g of the next i n u n d a t i o n . To consider this special activity m o d e in the respiration
m e a s u r e m e n t s , the animals were kept at low-tide conditions before the e x p e r i m e n t
started. Respiration m e a s u r e m e n t s were carried out for the duration of the m e a n n a t u r a l
i n u n d a t i o n period. For conversion of 1 ml 02 in g C a n oxicaloric e q u i v a l e n t of 4687 cal
per ml 02 was assumed, corresponding to 0.38 g C per ml 02.
The size-specific energy flow of the entire m a c r o f a u n a was estimated from the sum of
both secondary production a n d respiration per square metre a n d year for e v e r y size r a n g e
expressed in g C.
RESULTS
S i z e - f r e q u e n c y h i s t o g r a m of m a c r o f a u n a l b i o m a s s
The size-frequency histogram of macrofaunal biomass showed a b i m o d a l curve in
the Nereis-Corophium-belt, the s e a g r a s s - b e d a n d the Arenicola-flat (Fig. 1). M a x i m u m
biomass was found in a size group of i n d i v i d u a l weights of 0.18 to 0.32 m g AFDW in the
three communities. This size group consisted m a i n l y of the small p r o s o b r a n c h Hydrobia
ulvae. In the seagrass-bed, this m a x i m u m showed higher biomass v a l u e s t h a n in both
other communities. A second biomass p e a k was found at individual w e i g h t s of 10.00 to
17.78 mg AFDW in the Nereis-Corophium-belt, at individual w e i g h t s of 100.00 to
177.83 m g AFDW in the seagrass-bed, a n d of 316.22 to 562.34 m g AFDW in the
Arenicola-flat. In the Nereis-Corophium-belt, this second p e a k o r i g i n a t e d from the
polychaete Nereis diversicolor. In both other sand bottom communities, Arenicola marina
contributed most of the biomass within this size peak, showing a shift to a higher
individual weight due tb the longer i n u n d a t i o n of the Arenicola-flat. In the m u s s e l bed,
the size histogram of biomass was unimodal, showing a m a x i m u m at a size group of a n
individual weight of 0.562-1.0 g AFDW. This m a x i m u m was due to adult m u s s e l s Mytilus
edulis. The biomass-size histograms reveal a c h a n g e in d o m i n a n c e from small sized
macrofauna in shallow, shortly i n u n d a t e d parts of the tidal flat to the d o m i n a n c e of larger
m a c r o f a u n a n e a r the low tide level.
S i z e - f r e q u e n c y h i s t o g r a m s of s e c o n d a r y p r o d u c t i o n
Size-frequency histograms of the secondary production show a b i m o d a l p a t t e r n in
the three sand bottom c o m m u n i t i e s (Fig. 2) similar to the biomass-size spectra. In the
Arenicola-flat a n additional p e a k is found in the size class of 1.78- 3.16 m g AFDW, which
was formed by juveniles of the bivalve Macoma balthica. The highest p r o d u c t i o n was
found at the same individual size as the m a x i m u m biomass in the Nereis-Corophium-belt
Benthic grazers and suspension feeders
221
56 519//624
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20
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10
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!
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o.oool
N-C
o.ool
O.Ol
o,1
1.o
I n d i v i d u a l W e i g h t (g A F D W )
Fig. 1, Size-spectra of macrozoobenthic biomass (g AFDW m-2) and individual weight (g AFDW) of 4
intertidal macrofaunal assemblages of KSnigshafen. Biomass is indicated as the sum of total biomass
of macrofaunal species, averaged over one year, estimated for each size-class. N-C: NereisCorophium-belt; S: seagrass-bed; A: Arenicola-flat; M: mussel bed.
and the seagrass-bed, w h e r e a s in the Arenicola-flat this was found in a l o w er size r a n g e
(0.10 to 0.18 m g AFDW) than that of m a x i m u m biomass. This m ay be d u e to t h e g r e a t e r
a b u n d a n c e of juvenile I-Iydrobia ulvae, w h i c h t e n d to grow faster and thus will h a v e a
g r eat er production to biomass ratio than older and larger specimens. M a x i m u m production contributed to 51, 61 and 19 % to the total production of the N.C.-belt, the seagrassb e d an d the Arenicola-flat, respectively. As d e m o n s t r a t e d for biomass, the production of
this dominant size class was h i g h e s t in the seagrass-bed. Th e second p e a k of the
production-size curve was found at an individual w e i g h t of 31.62 to 56.24 m g (N.C.-belt),
222
H. A s m u s
29 j
YF
f
70 229'134
'~ 20-
5
M
o d_
o.oool
o.ool
Ind. W e i g h t
o.ol
o.1
Z
1.o
(g A F D W )
Fig. 2. Size-spectra of macrozoobenthic secondary production (g AFDW m -2 y - i ) and individual
weight (g AFDW) of 4 intertidal macrofaunal assemblages of K6nigshafen. Indicated values represent the sum of annual secondary production of each species estimated for each size-class. N-C:
1Vereis-Corophium-belt, S: seagrass-bed; A: Arenicola-flat; M: mussel bed.
100.00 to 177.83 m g (seagrass-bed) a n d 316.23 to 562.34 m g A F D W (Arenicola-flat). The
l o n g e r t h e i n u n d a t i o n time of the community, the h i g h e r the i n d i v i d u a l w e i g h t of animals
forming this p e a k . Additionally, the h e i g h t of production within this p e a k i n c r e a s e s in t h e
s a m e order. In the m u s s e l bed, 47 % of the s e c o n d a r y p r o d u c t i o n is f o r m e d b y the size
group of an i n d i v i d u a l w e i g h t of 562.34 to 1000.00 m g AFDW. This size g r o u p consisted
m a i n l y of a d u l t Mytilus edulis, but these mussels h a v e n l o w e r i n d i v i d u a l w e i g h t t h a n
those contributing to m a x i m u m biomass. Nevertheless, m a x i m u m p r o d u c t i o n is found in
the u p p e r r a n g e of the w h o l e size spectrum, r e v e a h n g a u n i m o d a l p r o d u c t i o n - s i z e histogram.
Macrofaunal respiration
The size h i s t o g r a m of m a c r o f a u n a l respiration reflects similar p a t t e r n s to those
o b s e r v e d in b i o m a s s a n d s e c o n d a r y production. The h i g h e s t respiration w a s f o u n d at the
Benthic grazers a n d suspension feeders
223
38 250/213
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r~
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0.0001
0.01
0.1
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1.0
Ind, W e i g h t ( g AFDW)
Fig. 3. Size-spectra of macrozoobenthic respiration (mg 02 m-2h -1) and individual weight (g AFDW)
of 4 intertidal macrofaunal assemblages of K6nigshafen. The respiration values indicate the sum of
the average respiration rate per hour of each species estimated for each size-class. N-C: NereisCorophium-belt; S: seagrass-bed ; A: Arenicola-flat; M: mussel bed.
lower size ranges in the three s a n d bottom communities (Fig. 3). Forty-two % of the total
macrofaunal respiration were used by Hydrobia ulvae of the size class of 0.10 to 0.18 mg
AFDW in the N.C.-belt. In the seagrass-bed a n d the Arenicola-flat, the m a x i m u m of
respiration (43 % a n d 27 %, respectively) originated from H. ulvae with a size of 0.18 to
0.32 mg AFDW. Nereis diversicolor (size range: 17.78 to 31.62 m g AFDW) caused a
second respiration p e a k in the N.C.-belt, a n d Arenicola marina (100.00 to 316.22 mg
AFDW) in the seagrass-bed ( 2.5 % ) a n d in the Arenicola-flat (3.2 %). B e t w e e n m a x i m u m
respiration at the lower size ranges a n d the second respiration peak, there was a n area of
m i n i m u m values r e s p o n d i n g to i n d i v i d u a l sizes of 1.78 to 10.00 m g AFDW. M a x i m u m
respiration (44 % of the total respiration) in the musseI b e d was found in the u p p e r size
range of adult M. edulis. The shape of the size-specific respiration curve was e q u i v a l e n t
to that of secondary production. M i n i m u m respiration was found at sizes of less t h a n
224
H. Asmus
0.32 m g AFDW. Total respiration was highest in the mussel b e d (1748 g C m -2 y-~)
followed b y the seagrass-bed (56 g C m -2 y-l), the Arenicola-flat (39 g C m -2 y - l ) and the
Nereis-Corophium-belt (24 g C m -2 y-t).
Size-specific e n e r g y flow
Total n e t e n e r g y flow of the communities decreased from the low-tide line to the
u p p e r shore. Highest values were estimated for the mussel b e d (2023 g C m -2 y - l ) a n d
the seagrass-bed ( 85 g C m -2 y - l ) . In the Arenicola-flat ( 69 g C m -2 y - l ) a n d in the N.C.belt (35 g C m -2 y - l ) e n e r g y flow was lower. Size-specific e n e r g y flow h a d a similar
bimodal shape as the spectra of biomass, secondary production a n d respiration for the
three sand bottom communities. E n e r g y flow of these communities can b e related to two
macrofaunal size groups. The first group consisted of small specimens, m a i n l y Hydrobia
ulvae, with a size r a n g e from < 0.10 to 1.78 m g AFDW. Within this group, the e n e r g y flow
was normally distributed over the entire size ranges. In the N.C-belt, the seagrass-beds
a n d the Arenieola-flat, respectively 93 %, 95 % a n d 78 % of the e n e r g y flowing through
the macrofauna was c o n c e n t r a t e d in this group. The share in e n e r g y flow of the second
group, with a size r a n g e larger t h a n 1.78 m g AFDW, was c o m p a r a b l y low. The e n e r g y
flow in this group increased from the N.C.-belt to the Arenicola-flat, s h o w i n g the
increasing importance of larger animals with longer i n u n d a t i o n times.
Mussel beds showed the m a x i m u m of e n e r g y flow in the u p p e r r a n g e of size
frequency. Mussel beds m a y control the e n e r g y flow of the total area, b e c a u s e t h e i r
e n e r g y flow per square metre surpassed the other communities by a n order of m a g n i t u d e .
This b e c a m e obvious by a comparison of the total e n e r g y flow of the different communities, taking into account their areal extension.
The total e n e r g y flow reflected the spatial extension (Table 1). A v e r a g e d over the
total area of K6nigshafen, the size-specific e n e r g y flow through the m a c r o f a u n a was
d e p e n d e n t on the extension of area covered by mussel beds. Because the area of mussel
beds fluctuates from year to year, a comparison of the total e n e r g y flow is m a d e b e t w e e n
a situation of 1 % (Reise et al., 1994) of the area of K6nigshafen covered b y m u s s e l beds
a n d 10 % coverage by mussel beds (Asmus & Asmus, 1990) (Fig. 4). Both cases showed a
b i m o d a l - s h a p e d curve. W h e n 1 % of the area is covered by mussels, the m a x i m u m of
e n e r g y flow is formed by the small macrofauna, the d o m i n a n t species b e i n g Hydrobia
ulvae. W h e n 10 % of the tidal flats are covered by mussels, the m a x i m u m of e n e r g y flows
through the larger macrofauna, the d o m i n a n t species b e i n g Mytilus eduIis.
DISCUSSION
U n i m o d a l a n d b i m o d a l size d i s t r i b u t i o n - W h a t a r e t h e e c o l o g i c a l effects?
The bimodal pattern of size histograms i n the three sand bottom c o m m u n i t i e s was
caused by two characteristic, clearly separated species groups. The s m a l l e r size group in
the r a n g e of 0.10 to 1.78 m g was d o m i n a t e d by Hydrobia ulvae, r e p r e s e n t i n g the trophic
type of browsers. Hydrobia ulvae m a i n l y grazes on diatoms a n d other m i c r o p h y t o b e n t h o s
(Fenchel & Kofoed, 1976; J e n s e n & Siegismund, 1980), which are p r o d u c e d in the same
habitat. The i m p o r t a n c e of a grazing food chain b a s e d on this browsing species for this
Benthic grazers a n d suspension feeders
225
117
//
20 84
i
J
'E
c~ 180
10% Mussel
Coverage
)h
~. 10b~
1% M . C .
olooo~ 01001
Ind. W e i g h t
o'.oi
o'.~
11o
(g AFDW)
Fig. 4. Total size-specific energy flow of the intertidal macrofauna of Kbnigshafen in relation to the
different percentages of areal coverage by mussel beds. The energy flow is estimated from the sum
of annual secondary production and annual respiration for each size group and represents the
amount of energy assimilated from the macrofauna. For the total energy flow, the per-unit-area
values of each assemblages were multiplied by the total areal coverage of the assemblage.
type of sandy intertidal flat was e m p h a s i z e d earlier (Asmus & Asmus, 1985). Extrapolating this to the total tidal flat: Kbnigshafen becomes a n ecosystem with a more or less
autochthonous e n e r g y flow. The e n e r g y a c c u m u l a t e d in this part of the f a u n a l assemblage is used only by a few e p i b e n t h i c invertebrate predator species hke shrimps
(Crangon crangon). M a n y authors describe shrimps feeding o n small rnacrofauna (Plagm a n n , 1939; Pihl & Rosenberg, 1984; Pihl, 1985; Reise, 1985; Beukema, 1992). Other
possible predators are juvenile shore crabs (Carcinus rnaenas) (Reise, 1978; Beukema,
1991) and, to a lesser extent, predatory gastropods (Retusa obtusa), n e m e r t i n e s a n d
predatory polychaetes (Reise, 1981).
It is u n k n o w n w h e t h e r small fish like the sand gobies feed on I-Iydrobia, b u t fish are
linked to this small m a c r o f a u n a group, by feeding on associated small polychaetes
(Pygospio elegans) a n d oligochaetes ( Tubificoides benedenii, Tubifex spec.) (Reise, 1978;
Wolff & Zijlstra, 1981; Raffaelh & Milne, 1987) a n d b y feeding on its predators, the p r a w n s
a n d amphipods (Raffaelh & Milne, 1987).
Animals in this size r a n g e may be too small for an effective predation b y most of the
226
H. Asmus
birds visiting the tidal flats. Shelducks (Tadorna tadorna) (Goethe,1980) a n d avocets
(Recurvirostra avosetta) are k n o w n to feed on Hydrobia ulvae, but these b i r d s are rare in
KSnigshafen. Zwarts & Blomert (1992) showed that an effective p r e d a t i o n by knots
(CaBdris canutus) starts at sizes in the u p p e r r a n g e of the size classes r e g a r d e d here as
the food web b a s e d on small macrofauna. Only a few species Like the d u n l i n (Cafidris
alpina) m a y use the total size spectrum of Hydrobia (Ehlert, 1964; H S f m a n n & Hoerschelm a n n , 1969; Glutz von Blotzheim et al., 1975; Mouritsen & Jensen, 1992). The quantitative assessment of how m u c h e n e r g y is transferred within this food w e b to higher trophic
levels is still u n k n o w n , but the n u m b e r of species which are able to profit from this group
of small-sized macrofauna seems to be limited. From the present results, it is possible to
estimate the a m o u n t of e n e r g y a n d material available from this group of m a c r o f a u n a to
the u p p e r trophic levels. L a u c k n e r (1986) reported that Hydrobia ulvae is i n some places
of KSnigshafen highly infected by parasites, b u t a quantification of this p~obably important b r a n c h of e n e r g y flow on the ecosystem level was not done.
The second distinctly s e p a r a t e d m a c r o f a u n a l group of the bimodal size histogram of
the animal a s s e m b l a g e was d o m i n a t e d by different species d e p e n d i n g o n habitat. In the
Nereis-Corophium-belt, this size group was formed by the polychaete Nereis diversicolor. This species has a wide r a n g e of f e e d i n g types, b e i n g omnivorous, detritivorous
a n d predatory (Hartmann-SchrSder, 1981). Because of its ability to form m u c u s nets as
particle traps, which are fed b y the worm w h e n it is filled, Nereis has the p o t e n t i a l to use
the water column as feeding habitat (Riisgard et ai., 1992). In both o t h e r s a n d bottom
assemblages, the seagrass-bed a n d the Arenicola-flat, Arenicola marina dominates this
second p e a k in the size spectrum of the assemblage. Arenicola m a i n l y f e e d s on the u p p e r
sediment layer (Fauchald & Jumars, 1979) but is also able to p u m p w a t e r through its
burrow (Krfiger, 1964; Jacobsen, 1967). The volume of water p u m p e d in this w a y is small
compared to the filtration capacity of a s u s p e n s i o n feeder [Baumfalk, 1979), b u t n e v e r t h e less the polychaete m a y exploit the water column for feeding.
The second p e a k in the m a c r o f a u n a size spectrum is d o m i n a t e d by species b e l o n g i n g
to another trophic type than those d o m i n a t i n g the food web b a s e d on small macrofauna.
These species are important prey organisms, especially for a large n u m b e r of w a d i n g
birds like bar-tailed godwits (Limosa lapponica) (Smith & Evans, 1973; Piersma et al.,
1980), curlews (Numenius arquata) (Boere & Smit, 1980}, dunlins (Calidris alpina), redshanks (Tringa totanus),*and oyster catchers (Haematopus phaeopus), that visit the tidal
flats of K6nigshafen frequently. Predation by fish is probably less i m p o r t a n t for the "large
food web", b e c a u s e most of the species are endobenthic, but predation o n syphon tips,
tail ends a n d other r e g e n e r a b l e parts of the body contribute to a c o n s i d e r a b l e a m o u n t to
the diet of some predators (de Vlas, 1979). The a m o u n t of e n e r g y or m a t e r i a l available
from this part of the faunal a s s e m b l a g e s increases with increasing i n u n d a t i o n time.
Whether this is a c o n s e q u e n c e of d e c r e a s i n g bird predation, or i n c r e a s i n g food supply
d u e to increasing i n u n d a t i o n time, is not clear. Considering the trophic role of the
W a d d e n Sea, the larger b e n t h i c species are generally regarded as the b a s e of the food
web of the ecosystem (Beukema, 19811. However m the sand bottom habitats of
K6nigshafen, this part of the b e n t h i c c o m m u n i t y contributes only 10 to 30 % to the total
energy flow.
Unimoclal size-frequency histograms of biomass, secondary production a n d respiration were f o u n d at all sites of m u s s e l b e d s in K6nigshafen. The m a x i m u m of the size
Benthic grazers a n d suspension feeders
227
s p e c t r u m was formed b y the large Mytilus edulis in the size r a n g e of 0.56 to 1.00 g. Size
s p e c t r a of b i o m a s s a n d s e c o n d a r y production are discussed in A s m u s (1987). M a i n
p r e d a t o r s on mussels in this s i z e - r a n g e are oystercatchers (Haematopus ostralegus) a n d
E i d e r d u c k s (Somatena mollissima). Because of the d o m i n a n c e of the blue m u s s e l in this
a s s e m b l a g e , s u s p e n s i o n feeding is the m a i n m o d e of e n e r g y acquisition for the macrofaunal a s s e m b l a g e . M o r e than the other a s s e m b l a g e s , the mussel b e d s d e p e n d on p e l a g i c
p r i m a r y production a n d p e l a g i c particle import (Asmus & Asmus, 1990). The b i o m a s s
m a x i m u m , as well as the m a x i m a for s e c o n d a r y production a n d respiration, surpass the
b i o m a s s p e a k at a similar size-class of the s a n d bottom a s s e m b l a g e s .
Barry & T e g n e r (1990) discuss the possible d e m o g r a p h i c b a c k g r o u n d l e a d i n g to
b i m o d a l or u n i m o d a l size-frequency distribution within a population. In a model, t h e y
s h o w e d that the p a t t e r n of a size-frequency histogram is mainly i n f l u e n c e d b y the
mortality rate a n d the growth rate. U n d e r the a s s u m p t i o n that these p a r a m e t e r s , as well
as the recruitment, are constant, no b i m o d a l or u n i m o d a l shapes of the size-distributions
are possible. Shifts in the ratio of mortality to growth with a g e from a g r o w t h - d o m i n a t e d
to a m o r t a l i t y - d o m i n a t e d population result in a strongly unimodal s i z e - f r e q u e n c y distribution. Stable b i m o d a l distributions require shifts from m o r t a h t y - d o m i n a t e d to growthd o m i n a t e d conditions via a g e - r e l a t e d c h a n g e s in mortality or growth, or both. Nonequilibrium conditions or events such as pulses in recruitment or mortality can also
modify size-frequency distributions, but these effects are usually transient. In contrast to
populations, size-specific growth a n d mortality in a s s e m b l a g e s are additionally v a r i a b l e
d u e to different rates of species a n d ages. These results indicate that inferences concerning the d e m o g r a p h i c dynamics are more difficult to derive from observing the s h a p e of
size-distribution on the a s s e m b l a g e level c o m p a r e d to the p o p u l a t i o n level.
This study d e m o n s t r a t e s that on the s a n d y tidal fiats of K6nigshafen, the m a c r o f a u n a l
a s s e m b l a g e is formed b y two s e p a r a t e size-groups with different ecological effects on the
total ecosystem, b e c a u s e both groups use different e n e r g y sources a n d direct t h e e n e r g y
into different p a t h w a y s . The habitat of a mussel b e d is d o m i n a t e d b y s u s p e n s i o n f e e d e r s
o c c u p y i n g the total s i z e - r a n g e of the a s s e m b l a g e .
S i z e - d i s t r i b u t i o n a n d t i d a l l e v e l : a k e y to e n e r g y u s e of a c o m m u n i t y ?
T h e size-distribution of b~omass a n d s e c o n d a r y production varies a m o n g the different a s s e m b l a g e s of a tidal flat. A simple a n d w i d e s p r e a d explanation is to refer i n c r e a s e s
in biomass and s e c o n d a r y production of populations - from the h i g h - t i d e h n e to the lowtide line - to the i n c r e a s i n g e n e r g y availabihty d u e to inundation. H a r v e y & Vincent
(1990) s h o w e d h i g h e r growth of Macoma balthica at levels with l o n g e r i n u n d a t i o n times:
additional growth differences within the size r a n g e of the population w e r e obvious from
the high- to Iow-tide hne.
In the p r e s e n t study, the small m a c r o f a u n a r e v e a l e d a m a x i m u m e n e r g y flow in the
s e a g r a s s - b e d e c o s y s t e m situated at the u p p e r part of the tidal flat, w h e r e a s n e a r the lowtide line, biomass a n d s e c o n d a r y production of this group w e r e less important. For the
food w e b b a s e d on small macrofauna, the e n e r g y availability seems, therefore, to b e
i n d e p e n d e n t of the tidal level, b e c a u s e this food w e b is b a s e d on g r a z i n g of microphytobenthos, w h i c h is h i g h e r in s e a g r a s s b e d s b y the additional availability of e p i p h y tes. E d g a r (1990b) also found an i n c r e a s e in b i o m a s s a n d s e c o n d a r y production d u e to the
228
H. A s m u s
i n c r e a s e of p l a n t m a t e r i a l in s e a g r a s s - b e d s , b u t he r e l a t e d the e l e v a t e d b i o m a s s v a l u e s to
the h i g h e r a v a i l a b i h t y of detritus from d e c a y i n g plants. Most of the s e a g r a s s - b e d s in
Kbnlgshafen are formed b y p o p u l a t i o n s of Zostera noltii, g r o w i n g on s a n d y s e d i m e n t s
with v e r y low shares of p l a n t detritus (Wille, pers. comm.). The h i g h e r b i o m a s s of smallsized m a c r o f a u n a in s e a g r a s s - b e d s m a y b e d u e to b e t t e r grazing conditions in the first
p l a c e a n d s e c o n d l y to protection from p r e d a t i o n (Reise, 1978) a n d t u r b u l e n c e . T u r b u lence a n d currents m a y b e the reason for worse g r a z i n g conditions in t h e d e e p e r tidal
levels, b e c a u s e s e d i m e n t stability is low; thus, growth conditions for m i c r o p h y t o b e n t h o s
are not as g o o d as in the u p p e r tidal flat (de Jonge, 1992) despite g o o d l i g h t conditions.
T h e large m a c r o f a u n a shows an i n c r e a s e in biomass, s e c o n d a r y p r o d u c t i o n a n d
e n e r g y flow with i n c r e a s i n g i n u n d a t i o n period. W h e n going down the shore, the dominant species, a n d a c c o r d i n g l y the d o m i n a n t f e e d i n g type, c h a n g e s from omnivorous to
s u s p e n s i o n feeding. In m u s s e l beds, b i o m a s s a n d s e c o n d a r y production as well as e n e r g y
flow show m a x i m u m d e v e l o p m e n t .
Grazers or suspension feeders: which one assumes the energetic dominance
the ecosystem level?
at
The g r a z i n g food chain is an i m p o r t a n t e n e r g y p a t h w a y on t h e tidal flats of
Kbnigshafen (Asmus & Asmus, 1985). Most of the a r e a is d o m i n a t e d b y g r a z i n g animals
like Hydrobia ulvae. H o w e v e r , m u s s e l b e d s surpass these areas b y b i o m a s s a n d secondary production p e r u n i t - a r e a {Asmus, 1987; A s m u s & Asmus, 1990). T h e e n e r g e t i c
d o m i n a n c e of one of t h e s e groups d e p e n d s on the areal extension of t h e a s s e m b l a g e .
Mussel b e d s s h o w l a r g e variations in a r e a l c o v e r a g e a n d biomass from y e a r to y e a r
(Dankers & Koelemaij, 1989). In K6nigshafen, m u s s e l b e d s occupy a b o u t 1 % (Reise, pers.
comm.) to 10 % (Asmus & Asmus, 1990) of the total area. The net e n e r g y flow (assimilated
energy) r e l a t e d to the total tidal flat i n c r e a s e s with an i n c r e a s i n g share of a r e a l c o v e r a g e
by m u s s e l b e d s from 94 g C m -2 y-1 at 1 % c o v e r a g e to 296 g C m -2 y - t a t a I 0 % cover.
Additionally, a shift from a w e a k e n e r g e t i c d o m i n a n c e of small m a c r o f a u n a to a distinct
e n e r g e t i c d o m i n a n c e of l a r g e m a c r o f a u n a is obvious. An increase in e n e r g y flow s e e m s to
b e possible only b y a s u p p o r t of food s u p p l y from outside Kbnigshafen.
CONCLUSIONS
Macrofaunal assemblages of the Nereis-Coroph~'um-belt, the seagrass-bed and the
Arenicola-flat each consisted of two groups, indicated by corresponding peaks in the size
spectra of biomass, secondary production, respiration and energy flow.
The first size-group was mainly made up of Hydrobia ulvae. Because of the small
size, this part of the assemblage may be effectively utilized by a hmited species number
Of small waders, whereas the main energy flow is directed via predation by shrimps
(Crangon crangon) to fishes. This food web is based on autochthonous primary production.
The s e c o n d size group can b e directly u s e d b y a lot of w a d i n g b i r d s a s well as b y
oystercatchers a n d e i d e r d u c k s . Biomass as well as s e c o n d a r y production, r e s p i r a t i o n a n d
e n e r g y flow of this food w e b b a s e d on l a r g e m a c r o f a u n a i n c r e a s e from t h e h i g h - f i d e line
down to the low-tide line. This food w e b is b a s e d on different e n e r g y sources from
Benthic grazers and suspension feeders
229
b e n t h i c a n d p e l a g i c p r o d u c t i o n as w e l l as f r o m d e t r i t u s i n p u t f r o m o u t s i d e t h e h a b i t a t .
M u s s e l b e d s a r e d o m i n a t e d b y this f o o d w e b , s u r p a s s i n g t h e o t h e r b e n t h i c a s s e m b l a g e s
in b i o m a s s a n d e n e r g y f l o w b y a n o r d e r of m a g n i t u d e . T h e e n e r g y f l o w of m u s s e l b e d s is
b a s e d o n e n e r g y s o u r c e s f r o m p h y t o p l a n k t o n p r o d u c t i o n a n d is t h u s d e p e n d e n t u p o n
i n p u t f r o m d e e p e r w a t e r s . T h e a m o u n t of t o t a l e n e r g y a s s i m i l a t e d b y t h e i n t e r t i d a l
m a c r o f a u n a of K 6 n i g s h a f e n d e p e n d s o n t h e e n e r g e t i c d o m i n a n c e of m u s s e l b e d s w i t h i n
the macrofaunal assemblages. A high areal coverage by mussel beds increases the
e n e r g y flow t h r o u g h t h e m a c r o f a u n a a n d i n d u c e s a shift f r o m a u t o c h t h o n o u s to a l l o c h thonous energy sources.
Acknowledgements, I am grateful for the kind help of my wife Ragnhild Asmus in all stages of this
work, from measurements to the final corrections of the manuscript. This work was supported by the
Deutsche Forschungsgemeinschaft (As 49/1-1) and by the Federal Ministry for Research and
Technology. This is publication no. 129 of the project "Ecosystem Research Wadden Sea".
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