Marine Biology 30, 119-128
@
by S p r i n g e r - V e r l a g 1975
(1975)
Particle Size-Selection of Two Deposit Feeders:
the Amphipod Corophium volutator and the Prosobranch
Hydrobia ulvae
T. Fenchel 1 , L. H. Kofoed I and A. Lappalainen 2
1 Department of Ecology, University of Aarhus; .~,rhus C, Denmark and
2Zoologiska Station Tv~rminne; Tv~irminne, Finland, and Bothnian Bay Research Institute, University of Oulu; Oulu, Finland
Abstract
The feeding biology of the d e p o s i t - f e e d i n g amphipod Corophium volutator is compared to
that of the coexisting, d e p o s i t - f e e d i n g p r o s o b r a n c h Hydrobia ulvae. R e g a r d i n g
ingestion of particles, both forms show size selection which alone can explain their
coexistence. Particle size-selection also explains some qualitative differences in
the c o m p o s i t i o n of the food of the two forms; thus, diatoms play a relatively
larger role in the diet of H. ulvae than in the diet o f c. volutator, whereas bacteria are probably relatively more important for the latter. Results of experiments with feeding of C-14 labelled microorganisms are in accordance w i t h the
findings on particle s i z e - d i s t r i b u t i o n of the gut contents, and show that (I)
c. volutator can only utilize b a c t e r i a adsorbed to particles within the size range
4 to 63 um (this is why the presence of clay and silt particles in the sediment
are n e c e s s a r y for efficient feeding of this amphipod); (2) c. volutator can utilize
bacteria suspended in the water pumped through its burrow for respiration if silt
and clay particles are present in the sediment. (3) H. ulvae can utilize large
particles, and also browses on surfaces, and some evidence is brought forward that
it also utilizes mucus for trapping microorganisms. The coexistence of depositfeeding animals is discussed. It is concluded that the number of coexisting,
closely related species is usually small, and that their resource p a r t i t i o n i n g is
probably mainly based on p a r t i c l e - s i z e selectivity. In the case of unrelated forms
(e.g.H. ulvae and C. volutator, a number of behavioural, physiological and morphological differences, and also the w i d e s p r e a d ability of deposit feeders to utilize
alternative feeding mechanisms may also lead to resource partitioning. Thus, there
are often several niche dimensions related to feeding allowing a certain diversity
of coexisting deposit feeders.
Introduction
Deposit or detritus feeders, i.e., animals which more or less indiscriminately
ingest their substrate, constitute an
important and often dominating part of
the larger invertebrates living in or
on sediments. The ecology and energetics of feeding of these animals have
attracted much interest. Evidence has
accumulated that they mainly utilize
the living components of the ingested
sediment -- bacteria, fungi, microalgae
and the m i c r o f a u n a -- whereas the bulk
of dead organic material of the sediments, w h i c h mainly consists of structural carbohydrates and other difficult
decomposable materials, is mainly
utilized indirectly through m i c r o b i a l
decomposers (Newell, 1965, 1970; F e n -
chel, 1970, 1972; Hylleberg Kristensen,
1972; and papers cited therein).
Less consideration has been given to
problems regarding coexistence and
competitive interactions. Levinton
(1972), from various evidence, concludes that communities of detritus
feeders constitute stable, food-limited
systems of "K-strategists", in which
competition would be important.
Few authors have so far attempted to
carry out experimental studies or to
analyse the mechanisms allowing coexistence of d e p o s i t - f e e d i n g animals.
M a n g u m (1964) and Reid and Reid (1969)
studied species of maldanids and of the
genus Macoma, respectively, and could
demonstrate several ecological differences between the species within
these two groups of related species.
120
T. Fenchel et al. : Particle Size-Selection of two Deposit Feeders
H o w e v e r , m o s t of these d i f f e r e n c e s
r e f e r r e d to h a b i t a t s e l e c t i o n and, w h e r e
food s e l e c t i v i t y was d e m o n s t r a t e d , no
a t t e m p t s to a n a l y s e w h e t h e r these differences could explain coexistence
w e r e made.
L a t e r p a p e r s w i l l deal w i t h the
distribution, coexistence, habitat
s e l e c t i o n , c o m p e t i t i v e e x c l u s i o n , and
c h a r a c t e r d i s p l a c e m e n t of the 4 s p e c i e s
of h y d r o b i i d snails o c c u r r i n g in D a n i s h
w a t e r s . The p r e s e n t p a p e r w i l l d e s c r i b e
p a r t i c l e s i z e - s e l e c t i o n and f e e d i n g
m e c h a n i s m s of the a m p h i p o d Corophium
volutator as c o m p a r e d to the p r o s o b r a n c h
Hydrobia ulvae, w i t h w h i c h c. volutator
c o e x i s t s in the s t u d i e d area, as is
o f t e n the case in s h a l l o w w a t e r of
n o r t h e r n Europe. The d i s t r i b u t i o n ,
b e h a v i o u r , and g e n e r a l b i o l o g y are w e l l
d e s c r i b e d in M e a d o w s and Reid (1966),
Muus (1967), and N e w e l l (1970). Both
forms are k n o w n d e p o s i t feeders; t h e i r
f e e d i n g is e a s i l y o b s e r v e d in the
l a b o r a t o r y and t h e i r guts are u s u a l l y
f i l l e d w i t h s e d i m e n t p a r t i c l e s , the
a t t a c h e d m i c r o f l o r a of w h i c h is a s s u m e d
to be u t i l i z e d . In addition, f i l t e r f e e d i n g has b e e n s u g g e s t e d for c. volutator, and h y d r o b i i d s are o f t e n o b s e r v e d
b r o w s i n g o n the t h a l l u s of ~ v a spp. and
o t h e r objects. Finally, it has b e e n
s u g g e s t e d that H. ulvae, w h i c h is often
found f l o a t i n g on the w a t e r surface,
can trap s u r f a c e - f i l m b a c t e r i a w i t h
s e c r e t e d m u c u s w h i c h is then later
e n g u l f e d . For b o t h forms, d i a t o m s are
o f t e n s t r e s s e d as i n g e s t e d p a r t i c l e s
of n u t r i t i v e value, but o t h e r m i c r o o r g a n i s m s w h i c h c a n n o t be i d e n t i f i e d
in the gut p r o b a b l y p l a y a s i m i l a r role,
a c c o r d i n g to t h e i r f r e q u e n c y in the
s e d i m e n t ingested.
Materials and Methods
Sampling Locality
The l a r g e r p a r t of this s t u d y was
c a r r i e d out in J a n u a r y , 1974 at the
Aarhus University Marine Biological
L a b o r a t o r y at R ~ n b j e r g H a r b o u r , Limfjorden, n o r t h e r n J u t l a n d ; some addit i o n a l e x p e r i m e n t s w e r e m a d e at the
D e p a r t m e n t of E c o l o g y in ~rhus. The
m a t e r i a l for the s t u d y was c o l l e c t e d
at " L e n d r u p Strand" a b o u t 6 km n o r t h
of the m a r i n e l a b o r a t o r y in a small
cove (about 750 x 250 m, a v e r a g e d e p t h
0.5 m) in the o p e n i n g of an a r t i f i c i a l
channel. The s a l i n i t y v a r i e s b e t w e e n
9 and 28~. The s e d i m e n t c o n s i s t s of
fine sand w i t h a m e d i a n g r a i n size of
a b o u t 140 pm, and w i t h 5% silt and clay
(i.e., p a r t i c l e s < 63 um). The m a c r o -
fauna is d o m i n a t e d by Corophium volutator
(10800 i n d i v i d u a l s / m z as b a s e d on 20
q u a n t i t a t i v e core samples taken in
F e b r u a r y , 1974) and two Hydrobia s p e c i e s
H. ventrosa (I 7 3 0 0 / m 2) and H. ulvae
(3060/m2). Also, the p o l y c h a e t e s Nereis
diversicolor and Polydora sp. and the
b i v a l v e s Mya arenaria and Cardium sp. are
common. The c. vOlutator p o p u l a t i o n
f l u c t u a t e s t h r o u g h the y e a r in a c c o r d a n c e w i t h its r e p r o d u c t i o n in e a r l y
summer; the other c o m p o n e n t s of the
fauna s e e m r e l a t i v e l y c o n s t a n t t h r o u g h out the year. The size range of H. ulvae
used in the p r e s e n t study was 4 to 6 mm,
and that of C. volutator 6 to 12 m m in
length. In the p r e s e n t study, only
H.
ulvae
was used in e x p e r i m e n t s for comp a r i s o n w i t h the p a r t i c l e i n g e s t i o n of
c. volutator. H o w e v e r , the g e n e r a l results
of this p a p e r r e g a r d i n g c o m p a r i s o n s of
c. volutator w i t h H. ulvae are also v a l i d
for H. ventrosa.
-
-
Particle Size-Distribution
of Ingested Material
In o r d e r to find the p a r t i c l e sized i s t r i b u t i o n of i n g e s t e d m i n e r a l p a r t i cles and d i a t o m s , w h o l e a n i m a l s coll e c t e d and p r e s e r v e d in the field or
a n i m a l s w h i c h had b e e n a l l o w e d to
e s t a b l i s h t h e m s e l v e s for at least 24 h
in trays w i t h n a t u r a l s e d i m e n t in the
l a b o r a t o r y w e r e c a r e f u l l y r i n s e d for
a d h e r i n g p a r t i c l e s ; in the case of
snails, these w e r e r e m o v e d from their
shell w h i c h often c o n s t i t u t e s a substrate for diatoms. The a n i m a l s w e r e
then p l a c e d in c e n t r i f u g e g l a s s e s w i t h
5-ml c o n c e n t r a t e d HNO 3, and the glasses
p l a c e d in a w a t e r b a t h at 90~
in the
h o o d for 2 h. The r e m a i n i n g p a r t i c l e s ,
w h i c h all d e r i v e d from the gut contents,
w e r e r i n s e d in d i s t i l l e d w a t e r twice
and then in ethyl a l c o h o l by s u c c e s s i v e
c e n t r i f u g a t i o n s , and f i n a l l y m o u n t e d on
m i c r o s c o p i c slides in p o l y v i n y l l a c t o phenol. V e r y o f t e n the gut m a t e r i a l ,
e s p e c i a l l y of Corophium volutator, did not
s e p a r a t e d u r i n g H N O 3 - t r e a t m e n t , but had
to be s p r e a d w i t h a n e e d l e on the slide
p r i o r to m o u n t i n g . O b s e r v a t i o n s on intact gut c o n t e n t s s h o w e d the v o l u m e
loss to be small, and that the g r e a t e s t
part of the v o l u m e of the gut c o n t e n t s
of l i v i n g a n i m a l s c o n s i s t s of m i n e r a l
p a r t i c l e s and s i l i c a frustules. U n d e r
400 x m a g n i f i c a t i o n , the d i a m e t e r of a
n u m b e r of r a n d o m l y s e l e c t e d p a r t i c l e s
w e r e t h e r e a f t e r m e a s u r e d w i t h an o c u l a r
m i c r o m e t e r to the c l o s e s t 2.5 pm. The
l e n g t h of d i a t o m frustules, and in two
cases also of the c h i t i n w a l l s of
fungal h y p h a e w h i c h a p p a r e n t l y are not
d i s s o l v e d in the n i t r i c acid, w e r e
T. Fenchel et al. : Particle Size-Selection of two Deposit Feeders
m e a s u r e d in a s i m i l a r way. The r e l a t i v e
v o l u m e of p a r t i c l e s of d i f f e r e n t sizes
w a s e s t i m a t e d as the t h i r d p o w e r of the
d i a m e t e r . T h i s p r e s u p p o s e s that p a r t i c l e s of d i f f e r e n t sizes h a v e s i m i l a r
shapes, w h i c h is p r o b a b l y not the case.
Also, the r e l a t i v e l y rare, l a r g e r
p a r t i c l e s c o n s t i t u t e an u n p r o p o r t i o n a t e l y large share of the t o t a l v o l u m e ,
m a k i n g the m e a s u r e m e n t of a large n u m ber of p a r t i c l e s n e c e s s a r y . It was
found t h a t m e a s u r e m e n t of 200 to 400
p a r t i c l e s gave r e a s o n a b l y r e p r o d u c i b l e
r e s u l t s and t h a t g r a i n - s i z e d i s t r i b u tion of n a t u r a l s a m p l e s of sand m e a s u r e d
in this w a y c o r r e s p o n d e d f a i r l y w e l l
w i t h r e s u l t s o b t a i n e d by w e t - s i e v i n g of
l a r g e r s a m p l e s and w e i g h i n g of the size
fractions.
Feeding Experiments with Labelled Microorganisms
For t r a c e r s t u d i e s w i t h l a b e l l e d m i c r o o r g a n i s m s , a n u m b e r of b a c t e r i a and
fungi w e r e i s o l a t e d from the sediment;
of these, two s t r a i n s of b a c t e r i a
(Strain d, a b o u t 4 um long, m o b i l e
v i b r i o s , f o r m i n g white, c o n v e x c o l o n i e s
on a g a r p l a t e s b a s e d on sea w a t e r enr i c h e d w i t h m i n e r a l s and w i t h s u s p e n d e d
c h i t i n as c a r b o n source; and S t r a i n g,
1 um long, m o b i l e rods, f o r m i n g w h i t e ,
c o n v e x c o l o n i e s on a g a r - a l g i n a t e sea
w a t e r p l a t e s on w h i c h it was i s o l a t e d
and grown) and a fungus (fb, an asc o m y c e t e f o r m i n g g r e e n - b l a c k spores and
grown on a g a r - a l g i n a t e sea w a t e r plates)
w e r e u s e d for the e x p e r i m e n t s . In o r d e r
to o b t a i n large n u m b e r s of cells for
e x p e r i m e n t s , i n o c u l a t e s of the s t r a i n s
w e r e t r a n s f e r r e d to 3OO-ml flasks w i t h
an a u t o c l a v e d n u t r i e n t b r o t h (3 g B a c t o b e e f e x t r a c t and 5 g B a c t o - t r y p t o n e / l
sea w a t e r ) . T h e s e l i q u i d c u l t u r e s w e r e
then u s e d a f t e r I to 3 days at 25~
P r i o r to the e x p e r i m e n t ,
1-ml 10 uCi
C-14 g l u c o s e s o l u t i o n w a s a d d e d to the
culture. A f t e r 10 m i n s h a k i n g at r e g u lar i n t e r v a l s , the c u l t u r e s w e r e cent r i f u g e d and r i n s e d in s t e r i l e sea
w a t e r twice. A f t e r a t h i r d c e n t r i f u g a t i o n and r e m o v a l of the s u p e r n a t a n t
t h e y w e r e r e a d y for use. E a c h e x p e r i m e n t u s u a l l y l a s t e d only 30 to 40 min;
d u r i n g this period, the loss of activity of the b a c t e r i a was less t h a n 10%.
The u n i d e n t i f i e d p e n n a t e d i a t o m s
o r i g i n a l l y i s o l a t e d from e s t u a r i n e sedim e n t s (A2, l e n g t h a b o u t 40 um and A30,
l e n g t h a b o u t 25 um) h a d b e e n grown
a x e n i c a l l y in s t o p p e r e d 5 O O - m l flasks
w i t h e n r i c h e d sea w a t e r and 4 uCi C-14
HCO~ u n d e r f l u o r e s c e n t light t u b e s for
s e v e r a l w e e k s b e f o r e the e x p e r i m e n t s .
P r i o r to the e x p e r i m e n t s , a k n o w n vol-
121
ume was c e n t r i f u g e d and the d i a t o m s
w e r e m i x e d into the s e d i m e n t w i t h a
s p a t u l a in the same w a y as for the
l a b e l l e d b a c t e r i a and fungi.
The e x p e r i m e n t s w h i c h s h o u l d d e m o n strate the s i g n i f i c a n c e of p a r t i c l e
s i z e - s e l e c t i o n w e r e all c a r r i e d o u t in
e s s e n t i a l l y the same way. To s m a l l
glass d i s h e s (3 cm d i a m e t e r , 3 cm high)
7 cm 3 sand w e r e added, e i t h e r n a t u r a l
sand or some s p e c i f i c p a r t i c l e - s i z e
fraction. 1-ml s u s p e n s i o n of e i t h e r
l a b e l l e d b a c t e r i a , fungi, or d i a t o m s
was m i x e d into the sand. IO-ml sea
w a t e r w e r e then added. At time zero,
20 Corophium volutator and 20 Hydrobia ulvae
w e r e added to each dish. The a n i m a l s
k e p t in f i l t e r e d sea w a t e r had b e e n
s t a r v e d for 2 to 3 h p r i o r to the exp e r i m e n t s , c. volutator u s u a l l y i m m e d i a t e ly b u r i e d t h e m s e l v e s into the s e d i m e n t
of the e x p e r i m e n t a l dishes; s o m e t i m e s
t h e y s t a r t e d to i n g e s t the s u r f a c e
s e d i m e n t w i t h o u t b u r r o w i n g , as a l s o
d e s c r i b e d by M e a d o w s and Reid (1966)
for s t a r v e d s p e c i m e n s . The s n a i l s
n o r m a l l y s t a r t e d to i n g e s t s e d i m e n t at
once; a few snails w o u l d u s u a l l y be
f o u n d f l o a t i n g in the s u r f a c e d u r i n g
the e x p e r i m e n t , b u t t h e y w e r e g e n t l y
p o k e d d o w n on the s e d i m e n t a g a i n w i t h
a spatula. Two or 5 m i n a f t e r s t a r t i n g
the e x p e r i m e n t , and a g a i n 4 times during the e x p e r i m e n t a l p e r i o d of 30 or
40 min (which is a p p r o x i m a t e l y the time
it takes for b o t h s p e c i e s to fill t h e i r
guts), 4 s p e c i m e n s of e a c h s p e c i e s w e r e
r e m o v e d for r a d i o a c t i v i t y counts.
U s u a l l y s e v e r a l e x p e r i m e n t s w e r e carr i e d out s i m u l t a n e o u s l y .
In o r d e r to s t u d y the a b i l i t y of
Corophium volutator to use s u s p e n s i o n s of
b a c t e r i a as food, the f o l l o w i n g e x p e r i m e n t was c a r r i e d out. To 4 c o n t a i n e r s ,
2 of w h i c h had a l a y e r of n a t u r a l sedim e n t on the b o t t o m , 20-ml sea w a t e r
w i t h I ml of a s u s p e n s i o n of C-14 labelledBacterium
d was added. Ten c.
volutator w e r e a d d e d to one c o n t a i n e r
with, and ten to one c o n t a i n e r w i t h o u t
sediment; the r e m a i n i n g 2 c o n t a i n e r s ,
one w i t h o u t , one w i t h s e d i m e n t , w e r e
u s e d as controls. At r e g u l a r i n t e r v a l s
(Fig. 7) 1-ml s a m p l e s w e r e t a k e n from
the c o n t a i n e r s , m e m b r a n e - f i l t e r e d ,
and
the a c t i v i t y m e a s u r e d .
C o u n t i n g was c a r r i e d out w i t h a GMcounter. The r a d i o a c t i v i t y of m i c r o b i a l
s u s p e n s i o n s was m e a s u r e d by f i l t e r i n g
I ml t h r o u g h 0.45 ~m m e m b r a n e f i l t e r s
f i t t i n g the p l a n c h e t t e s of the counter.
A f t e r r i n s i n g in sea w a t e r , w h o l e animals w e r e h o m o g e n i z e d in the p l a n c h e t t e s
in a d r o p of m e t h a n o l w i t h a spatula.
The "paste" was s p r e a d out e v e n l y on
the b o t t o m of the p l a n c h e t t e s , dried,
T. Fenchel et al. : Particle
122
Size-Selection
of two Deposit
Feeders
7~
80
80
60
60
z
40
&o
20
;~,
L
~_--~,
4
8
16
,
32
64
,
128 256
~.,-~-..
512
lu24pm
o
2
diameter
Fig. i P a r t i c l e - s i z e frequency (volume %) of
mineral p a r t i c l e s ingested by Corophium volutatot (filled circles) and Hydrobia ulvae (open
circles) and of natural sediment (dots). Each
curve represents gut contents b a s e d on p o o l e d
gut contents of iO specimens
cpm
4
8
16
32 64
length
128 256 512pm
Fig. 2. P a r t i c l e - s i z e frequency of diatoms
ingested by Corophium volutator and Hydrobia
ulvae and of diatoms in sediment. For further
e x p l a n a t i o n see legend to Fig. i
cpm
B
75
75
50
5O
25
25
I~)
2(3
3~3
40 min
0
1
20
30
40 rain
Fig. 3. Uptake of labelled b a c t e r i a (Strain g) by Corophium volutator (filled circles) and Hydrobia
ulvae (open circles) in two d i f f e r e n t sediments: (A) 250 to 500 pm ans fraction; (B) 250 to 500 pm
fraction with addition of 5% silt and ciay. cpm: counts/min
T. Fenchel et al. : Particle Size-Selection of two Deposit Feeders
r
100
8O
~o
2o
i
i
i
i
10
20
30
40
I
123
and counted. The standard deviation
of
c o u n t s of a n i m a l s w a s a b o u t Z 10%.
S i n c e t h i s s t u d y d i d n o t a t t e m p t to
make quantitative
measurements
of c o n s u m p t i o n r a t e s , b u t o n l y to c o m p a r e
efficiences
of t h e t w o f o r m s o f d e p o s i t
f e e d e r s as a f u n c t i o n of p a r t i c l e
size
a n d to d e s c r i b e q u a l i t a t i v e
a s p e c t s of
t h e i r f e e d i n g b i o l o g y , r e s u l t s are
s i m p l y g i v e n as c p m ( c o u n t s / m i n )
after
subtraction
of the b a c k g r o u n d .
No correction for self-absorption
was made,
as t h i s is a s s u m e d t o v a r y l i t t l e f r o m
s a m p l e to s a m p l e s i n c e t h e s e w e r e of
nearly the same thickness,
i.e., a r o u n d
I m g . c m -2 .
50 m[n
Fig. 4. Corophium volutator. Uptake of labelled
bacteria (Strain g) in 125 to 250 Hm sand
fraction with (open circles) and without
(filled circles) addition of 5% silt and clay
cpm
200
A
180
16O
l&O
120
100
80
60
Choice Experiments
with Corophium
volutator
Some simple experiments
were carried
o u t in o r d e r to s t u d y t h e a b i l i t y of
Corophium volutator to d i s c r i m i n a t e
between different
qualities
of sand. In
these experiments,
2 to 6 s m a l l d i s h e s
(3 x 3 cm), w i t h s a n d s of d i f f e r e n t
q u a l i t i e s w e r e p l a c e d in c r y s t a l l i z a tion dishes with 300-ml sterile sea
w a t e r a n d 15 or 20 c. volutator a d d e d .
A f t e r 2 or 3 h, t h e d i s h e s w e r e r e m o v e d
a n d t h e n u m b e r s of a m p h i p o d s
in e a c h
d i s h c o u n t e d . If a n y a t t r a c t i v e
sand
f r a c t i o n at all w a s p r e s e n t
(and t h e
amount offered was sufficiently
high
to p r e v e n t c o m p e t i t i o n
for space) at
m o s t I or 2 a n i m a l s w e r e s w i m m i n g a r o u n d
in t h e w a t e r at t h e e n d of t h e e x p e r i mental period.
40
Results
20
Particle Size-Distribution
J
1'0
2'0
30
50 rain
lOO
B
6O
4O
2O
~ ' - -
i
10
0
of Gut Contents
i
4'0
i
{
I
20
30
40
9
I
50rain
Fig. 5. Uptake of (A) labelled diatoms (A2),
and (B) bacteria (Strain d) by Corophium volutator (filled circles) and Hydrobia ulvae
(open circles) in 125 to 250 um sand fraction
without finer particles
Particle size-distribution
of t h e m i n eral particles
and diatom frustules
f r o m Corophium volutator and f r o m
Hydrobia
ulvae
w e r e m e a s u r e d on t h r e e o c c a s i o n s ,
as w e l l as the p a r t i c l e
size-distribut i o n s of t h e m i n e r a l p a r t i c l e s
a n d of
t h e d i a t o m s of t h e s e d i m e n t in w h i c h
the a n i m a l s h a d l i v e d for s e v e r a l d a y s
in a t r a y (Figs. I and 2)). B o t h f o r m s
i n g e s t a r a t h e r n a r r o w r a n g e of p a r t i c l e
size, w i t h l i t t l e o v e r l a p ; in c. volutator,
p a r t i c l e s b e t w e e n 4 a n d 60 ~m c o m p r i s e n e a r l y t h e t o t a l v o l u m e of t h e
g u t c o n t e n t , w h e r e a s in H. ulvae p a r t i c l e s b e t w e e n 20 a n d 2 0 0 - 3 0 0 ~m d o m i n a t e .
Fig. I w o u l d s u g g e s t t h a t H. ulvae ingests particles
in t h e p r o p o r t i o n
in
w h i c h t h e y o c c u r in t h e s u b s t r a t e .
This,
h o w e v e r , is n o t t h e rule; t h e p a r t i c l e
sizes ingested by hydrobiid
snails are
m a i n l y a f u n c t i o n of i n d i v i d u a l
animal
s i z e ( F e n c h e l , in p r e p a r a t i o n ) .
That
H. ulvae d o e s n o t i n g e s t p a r t i c l e s
in
124
T. Fenchel et al. : Particle Size-Selection of two Deposit Feeders
o
;70
cpm/rnt ~"-'---~o.~ ~
500
withoul sediment
-o
6OO
5OO
400
40O
b
3OO
300
2O0
I00~
200
,
i
i
i
3OO
'i
O0
200
f
Io
o
with sediment
100
[<.
60
q
50
100}
40
A2
30
0
40
30
.
bacter,um d
.... bocter[um g
i
,
10
Uptake of
i
i
20
30
5 different
40
50 min
Fig,
labelled
microorganisms in natural sand by Corophium volutator (filled circles) and Hydrebia u l v a e ( o p e n
circles). Triangles represent uptake of bacteria by H. ulvae in absence of sediment
proportion
to t h e i r o c c u r r e n c e
is o b vious from the ingested diatoms
(Fig. 2):
the dominating
d i a t o m s in t h e g u t c o n t e n t s a r e l a r g e r t h a n t h e d i a t o m s in
the sediment.
Feeding Experiments
i
50
" ~-~
f
%00
i
150
"~
9
|
200
i
250 min
jJ~oo_~~"
2C
0
6.
"
Fig. 7. Decrease of radioactivity of bacterial
suspension in presence of Corophium volutator
(filled circles) and in control experiments
(open circles)
lo
i
I
~
with Labelled Microorganisms
Figs. 3 and 4 show the ingestion
b a c t e r i a b y Corophium volutator a n d
of
Hydrobia
ulvae in s a n d s
(7 e m 3) w i t h e i t h e r a
particle-size
r a n g e of 250 t o 5 0 0 um o r
of 125 to 250 um, a n d w i t h o r w i t h o u t
t h e a d d i t i o n of a b o u t 0 . 3 c m 3 c l a y a n d
s i l t (i.e., < 62 um f r a c t i o n ) . T h e s e
experiments
r e v e a l t h a t c. volutator
is
d e p e n d e n t o n t h e p r e s e n c e of f i n e m i n eral particles
in o r d e r t o i n g e s t b a c teria. The most likely explanation
is
that bacteria adhere to the particles
which
c. volutator i n g e s t . T h e b a c t e r i a l
i n g e s t i o n o f H. ulvae
was not affected
b y t h e p r e s e n c e of f i n e p a r t i c l e s .
Fig. 5 s h o w s t h a t , i n 125 t o 250 ~m
sand,
Corophium volutator is a b l e t o
i n g e s t D i a t o m A2 ( 4 0 - u m long)
(Fig. 5A),
w h e r e a s it c a n n o t u t i l i z e b a c t e r i a in
the same sediment
(Fig. 5B). T h i s
demonstrates
t h a t c. volutator c a n f e e d
in t h e c o a r s e r s a n d f r a c t i o n if f o o d
particles within a suitable size range
a r e a v a i l a b l e , b u t in o r d e r t o u t i l i z e
b a c t e r i a t h e p r e s e n c e of m i n e r a l p a r t i c l e s < 60 um is n e c e s s a r y .
T. Fenchel et al. : Particle Size-Selection of two Deposit Feeders
Finally,
g e s t i o n of
in n a t u r a l
cality. For
Fig. 6 i l l u s t r a t e s the in5 different microorganisms
sand from the s a m p l i n g lor e a s o n s not u n d e r s t o o d ,
Corophium volutator a l w a y s s e e m e d to ingest less s u c c e s s f u l l y in n a t u r a l sand
than in the size f r a c t i o n 125 to 250 pm
w i t h about 5% clay and silt added. It
can be seen that the two d i a t o m s (both
w i t h i n the size r a n g e i n g e s t e d by b o t h
animals) and b a c t e r i a are i n g e s t e d w i t h
an e f f i c i e n c y ratio of Hydrobia ulvae to
C. velutator of about 4:1. This ratio
h o w e v e r , is d e p e n d e n t on the c o m p o s i t i o n
of the sand w h e n b a c t e r i a c o n s t i t u t e
the food o r g a n i s m s ; f u r t h e r m o r e , the
b a c t e r i a e a t e n by c. volutator are not
the same as those c o n s u m e d by H. ulvae,
i.e., the b a c t e r i a eaten by the f o r m e r
are those a d h e r i n g to small p a r t i c l e s ,
w h e r e a s t h o s e e a t e n by the l a t t e r are
m a i n l y a d h e r i n g to larger p a r t i c l e s .
W i t h r e g a r d to f u n g a l m y c e l i a , only
Hydrobia ulvae seems able to i n g e s t these;
this is u n d e r s t a n d a b l e , since even small
p i e c e s of m y c e l i a are larger than parcan
t i c l e s w h i c h Corophium volutator
handle. In some s a m p l e s of H. ulvae and
H. ventrosa
c o l l e c t e d and p r e s e r v e d in
the field in F e b r u a r y , a b o u t I to 2%
of the gut v o l u m e was m a d e up of fungal
m y c e l i a of the type used for the p r e s e n t
experiments.
Filter-feeding in Corophium volutator
The r e s u l t of the e x p e r i m e n t for t e s t i n g
the a b i l i t y of Corophium volutator to utilize s u s p e n d e d b a c t e r i a is shown in
Fig. 7. In the s y s t e m c o n t a i n i n g c. volutator
w i t h o u t s e d i m e n t no d e c r e a s e in
the s u s p e n d e d b a c t e r i a o c c u r r e d (the
s o m e w h a t m o r e r a p i d drop in r a d i o a c t i v ity in the c o n t r o l w i t h o u t s e d i m e n t was
p r o b a b l y due to some s e t t l e m e n t of bacteria b e i n g p a r t i a l l y p r e v e n t e d by
t u r b u l e n c e c r e a t e d by the a m p h i p o d s ) .
In the s y s t e m w i t h sediment, h o w e v e r ,
the b a c t e r i a l c o n c e n t r a t i o n of the w a t e r
in the c o n t a i n e r w i t h a m p h i p o d s had
fallen to a b o u t 40% of that of the control a f t e r 4 h. At the end of the exp e r i m e n t , the a m p h i p o d s in the s y s t e m
w i t h o u t s e d i m e n t w e r e only s l i g h t l y
r a d i o a c t i v e . In the s e d i m e n t s y s t e m the
tubes w e r e only s l i g h t l y r a d i o a c t i v e ,
w h e r e a s the a m p h i p o d s t h e m s e l v e s w e r e
c o n s i d e r a b l y m o r e active. J u d g i n g from
the counts, the r a d i o a c t i v i t y of the
a m p h i p o d s c o u l d a c c o u n t for about 20%
of the loss of a c t i v i t y in the water;
h o w e v e r , due to the facts that (I) the
a m p h i p o d s could, d u r i n g the 4 h, h a v e
e m p t i e d t h e i r guts s e v e r a l times, the
a s s i m i l a t i o n c o u l d not h a v e b e e n 1OO%,
125
and they w o u l d a l r e a d y h a v e r e s p i r e d
some of the C-14 a s s i m i l a t e d , and that
(2) no c o r r e c t i o n was m a d e for a h i g h e r
s e l f - a b s o r b t i o n of the p l a n c h e t t e s w i t h
a m p h i p o d s r e l a t i v e to that of d r i e d
filters w i t h b a c t e r i a , it is p r o b a b l e
that the a m p h i p o d s did i n g e s t a l a r g e r
p a r t of the b a c t e r i a than i n d i c a t e d by
the counts.
A l t h o u g h it can be a r g u e d that the
s p e c i m e n s in the s e d i m e n t - f r e e s y s t e m
w e r e u n a b l e to filter since they w e r e
not e s t a b l i s h e d in b u r r o w s , the fact
that Corephium volutator also c a n n o t ingest b a c t e r i a in s e d i m e n t s w i t h o u t a
clay and silt f r a c t i o n i n d i c a t e s that
also in the case of f i l t r a t i o n of susp e n d e d b a c t e r i a , a d s o r b t i o n to fine
m i n e r a l p a r t i c l e s is n e c e s s a r y p r i o r to
ingestion. It is, of course, h i g h l y
can d i r e c t l y
p r o b a b l e that c. volutator
u t i l i z e s u s p e n d e d p a r t i c l e s of a somew h a t larger size, e.g. small p l a n k t o n i c
algae.
A c c o r d i n g to M e a d o w s and Reid (1966),
the s o r t i n g of d e t r i t a l food takes
p l a c e on the setal b a s k e t f o r m e d by the
Ist and 2nd g n a t h o p o d s , t h r o u g h w h i c h
the r e s p i r a t o r y w a t e r c u r r e n t also
flows, w h e r e a s the r e m a i n i n g m o u t h app e n d a g e s p l a y a role in the t r a n s p o r t
of food and, to some extent, t r i t u r a tion; a c c o r d i n g to t h e s e authors, v e r y
small p a r t i c l e s pass t h r o u g h the b a s k e t
and larger sand grains are d i s c a r d e d .
P h o t o m i c r o g r a p h s t a k e n d u r i n g the
p r e s e n t i n v e s t i g a t i o n of the setae of
the 2nd g n a t h o p o d i n d i c a t e that the
fine b r i s t l e s form a r e g u l a r n e t w o r k
w h i c h w i l l r e t a i n p a r t i c l e s of > 4 um
or so. It is m o r e d i f f i c u l t to e v a l u a t e
the filter f o r m e d by the Ist g n a t h o p o d .
The setae of this a p p e n d a g e a p p e a r in
a thicker, l e s s - o r d e r e d layer, w i t h
s h o r t e r b r i s t l e s . However, also this
f i l t e r does not a p p e a r to be able to
r e t a i n b a c t e r i a , i.e., p a r t i c l e s w i t h
the size range I to 2 um.
Ability of Hydrobia ulvae to Ingest Bacteria
in Absence of Sediment
In c o n t r a s t to Corophium volutator, Hydrobia
ulvae
does a t t a i n a c e r t a i n r a d i o a c t i v ity w h e n p l a c e d in d i s h e s w i t h a susp e n s i o n of l a b e l l e d b a c t e r i a in the
a b s e n c e of sediment; in one case, m o r e
than 50% of the a c t i v i t y o b t a i n e d in
a p a r a l l e l e x p e r i m e n t w i t h n a t u r a l sedim e n t was r e c o r d e d (Fig. 6).
The m e c h a n i s m r e s p o n s i b l e for this
is p r o b a b l y the i n g e s t i o n of s e c r e t e d
m u c u s w h i c h has t r a p p e d b a c t e r i a , a
b e h a v i o u r p r e v i o u s l y s u g g e s t e d by o t h e r
a u t h o r s (see Newel!, 1970). As w i l l be
126
T. Fenchel et al. : Particle Size-Selection of two Deposit Feeders
s h o w n by K o f o e d (in press, b) Hydrobia
ulvae w i l l i n g l y b r o w s e s on b a c t e r i a
c o n c e n t r a t e d on m e m b r a n e - f i l t e r s , but it
seems i m p r o b a b l e that b r o w s i n g on surfaces on w h i c h o n l y a thin layer of
b a c t e r i a is a d s o r b e d (as m u s t h a v e b e e n
the case in our e x p e r i m e n t s ) c o u l d be
s u f f i c i e n t . H o w e v e r , this a s p e c t of the
f e e d i n g b i o l o g y of H. ulvae was not s t u d ied in f u r t h e r detail.
Choice Experiments with Corophium volutator
The e x p e r i m e n t s m a i n l y c o n f i r m the
f i n d i n g s of M e a d o w s (1964). T h e y all
c l e a r l y i l l u s t r a t e d the a b i l i t y of Corophium volutator to d i s c r i m i n a t e b e t w e e n
d i f f e r e n t k i n d s of sand. E x p e r i m e n t s
w i t h n a t u r a l sand from the s a m p l i n g
locality, various particle size-fractions of it, and c o m b i n a t i o n s of t h e s e
size fractions, s h o w e d that the p r e s e n c e
of p a r t i c l e s < 63 um made the sand
a t t r a c t i v e and that a m p h i p o d s w i l l not
b u r y in sands w h e r e the < 125 um fract i o n has b e e n r e m o v e d u n l e s s no o t h e r
a l t e r n a t i v e is offered, and even then
a large p r o p o r t i o n w i l l always be freeswimming. F u r t h e r m o r e , w h e n the c o a r s e r
f r a c t i o n s (> 250 um) w e r e r e m o v e d from
the sand from the s a m p l i n g l o c a l i t y it
b e c a m e m o r e a t t r a c t i v e than u n t r e a t e d
sand.
N a t u r a l sand was always p r e f e r r e d to
sand that had b e e n a u t o c l a v e d and k e p t
in s t e r i l e sea w a t e r for some time. The
l a t t e r w o u l d only a t t r a c t few i n d i v i d uals, even in the a b s e n c e of a l t e r n a tives. M i x i n g w i t h pure s t r a i n s of b a c t e r i a (d, g, and a few others) r e n d e r e d
the sand a t t r a c t i v e again, a l t h o u g h in
c h o i c e e x p e r i m e n t s w i t h n a t u r a l sand
the m a j o r i t y of a m p h i p o d s p r e f e r r e d
this to sand c o n t a i n i n g one kind of
b a c t e r i u m . M i x i n g d i a t o m s into autoc l a v e d sand did not alter its a t t r a c tability significantly, whether tested
a g a i n s t s t e r i l e sand, s t e r i l e sand plus
one type of b a c t e r i u m , or a g a i n s t natural sand, a l t h o u g h there was some
i n d i c a t i o n s that d i a t o m s plus s t e r i l e
sand was p r e f e r r e d to s t e r i l e sand.
S i m i l a r e x p e r i m e n t s w i t h Hydrobia ulvae
in P e t r i d i s h e s p a r t i t i o n e d into two
h a l v e s w i t h d i f f e r e n t kinds of sand in
e a c h c o m p a r t m e n t f a i l e d to r e v e a l any
a b i l i t y of the s n a i l s to d i s c r i m i n a t e
b e t w e e n any of the a b o v e - m e n t i o n e d
types of~sands.
Discussion and Conclusions
The n u m b e r of s p e c i e s w h i c h can c o e x i s t
in a s t a b l e c o m m u n i t y is, at most,
i d e n t i c a l to the n u m b e r of d i f f e r e n t
l i m i t i n g r e s o u r c e s , p r o v i d e d the s p e c i e s
d i s t i n g u i s h b e t w e e n them, i.e., u t i l i z e
the d i f f e r e n t r e s o u r c e s w i t h a diff e r e n t i a l e f f i c i e n c y or are able to
d i s c r i m i n a t e b e t w e e n t h e m (MacArthur
and L e v i n s , 1964). A l t h o u g h d e t r i t u s
f e e d e r s do in fact feed on a large
d i v e r s i t y of food o r g a n i s m s , it is unlikely that the a b i l i t y to u t i l i z e t h e m
in a d i f f e r e n t i a l w a y or to s p e c i a l i z e
on c e r t a i n types is w i d e s p r e a d , since
they i n g e s t t h e m t o g e t h e r w i t h the substrate in a s e e m i n g l y i n d i s c r i m i n a t e
manner. H a r g r a v e (1970) found that the
f r e s h - w a t e r a m p h i p o d Hyalella azteca ass i m i l a t e s r e p r e s e n t a t i v e s of q u i t e different m i c r o b i a l o r g a n i s m s (with the
e x c e p t i o n of b l u e - g r e e n algae) w i t h
a b o u t the same e f f i c i e n c y ; K o f o e d
(in press, a) r e p o r t e d that Hydrobia
ventrosa can u t i l i z e d i f f e r e n t s t r a i n s
of b a c t e r i a , b l u e - g r e e n s and d i a t o m s
w i t h about the same, high e f f i c i e n c y ,
and F e n c h e l (1970) also found this to
be the case for the a m p h i p o d parhyalella
whelpleyi.
The m e i o - and m i c r o f a u n a , w h i c h ess e n t i a l l y feed on the same food items
as do the d e t r i t u s - f e e d i n g m i c r o f a u n a ,
are able to s p e c i a l i z e on d i f f e r e n t
k i n d s and s i z e - g r o u p s of m i c r o o r g a n i s m s ,
and the high d i v e r s i t y of the m i c r o fauna -- a few cm 3 of sand m a y c o n t a i n
50 to 1OO s p e c i e s -- can l a r g e l y be exp l a i n e d by n i c h e d i v e r s i f i c a t i o n in
choice of food (Fenchel, 1969, and
r e f e r e n c e s therein). This f a u n a is thus
"coarse g r a i n e d " in the t e r m i n o l o g y
of M a c A r t h u r and L e v i n s (1964) as opp o s e d to the "fine grained" d e t r i t u s
feeders w h i c h do not d i s c r i m i n a t e bet w e e n d i f f e r e n t k i n d s of food p a r t i c l e s .
C o n s e q u e n t l y , the d i v e r s i t y of d e t r i t u s
feeders could be e x p e c t e d to be low on
any one h a b i t a t and, f u r t h e r m o r e , t h e i r
d i v e r s i t y w o u l d p r e s u m a b l y to a large
e x t e n t be b a s e d on h a b i t a t s p e c i a l i z a tion, e.g. a c c o r d i n g to salinity, type
of s u b s t r a t e , d e p t h (Kohn, 1971). Alt h o u g h the n u m b e r of c o e x i s t i n g d e t r i t u s
feeders u s u a l l y is low, s e v e r a l s p e c i e s
are n e v e r t h e l e s s o f t e n found t o g e t h e r
in the same l o c a l i t y w i t h o u t s h o w i n g
any o b v i o u s s p a t i a l z o n a t i o n p a t t e r n s .
The p r e s e n t i n v e s t i g a t i o n has shown
that the two s p e c i e s studied, p r o b a b l y
as a r e s u l t of t h e i r r e s p e c t i v e morp h o l o g i c a l s t r u c t u r e s , show p a r t i c l e
s i z e - s e l e c t i o n . A c c o r d i n g to e m p i r i c a l
f i n d i n g s on c o e x i s t i n g , c l o s e l y r e l a t e d
s p e c i e s as w e l l as t h e o r e t i c a l cons i d e r a t i o n s , the stable c o e x i s t e n c e
b a s e d on food s i z e - s e l e c t i o n alone
r e q u i r e s that the log m e a n sizes of the
i n g e s t e d p a r t i c l e s d i f f e r by s o m e w h a t
m o r e than one s t a n d a r d d e v i a t i o n (as-
T. Fenchel et al. : Particle Size-Selection
of two Deposit Feeders
s u m i n g log n o r m a l d i s t r i b u t i o n
of t h e
particle sizes eaten by the different
species; MacArthur,
1972, a n d r e f e r e n c e s
t h e r e i n ) . As s e e n f r o m Figs. I a n d 2,
this requirement
is s a t i s f i e d
in t h e
c a s e of Corophium volutator a n d Hydrobia
ulvae.
Particle size-selection
also has
more qualitative
a s p e c t s . In t h e s u r f a c e s e d i m e n t l a y e r (about 0 to 3 m m
depth) of the s e d i m e n t s on w h i c h t h e
g r a p h s in Figs. I a n d 2 a r e b a s e d ,
microscopical
measurements
on t w o o c c a s i o n s i n d i c a t e d t h a t 8.3 a n d 11.9%,
respectively,
of t h e v o l u m e w a s m a d e
up of d i a t o m s . In the g u t c o n t e n t s of
Hydrobia ulvae d i a t o m s m a d e up 29.6, 44.7
a n d 3 7 . 1 % of t h e v o l u m e ; in Corophium
volutator g u t c o n t e n t s , d i a t o m s c o n s t i t u t e d 4.0 a n d 2 1 . 5 % (in the t h i r d
case diatoms were not measured).
These
values constitute
an o v e r - e s t i m a t e
of d i a t o m s r e l a t i v e to s a n d g r a i n s ,
s i n c e t h e t h i r d p o w e r of t h e l e n g t h
w a s u s e d as t h e m e a s u r e for d i a t o m
volume; however,
it is c l e a r t h a t
diatoms must play a relatively
larger
r o l e in f e e d i n g of H. ulvae. T h e e n r i c h m e n t of d i a t o m s in t h e i n t e s t i n a l
cont e n t s of the s n a i l s r e l a t i v e to t h e
s e d i m e n t c a n be e x p l a i n e d
only by particle size-selection,
although a tend e n c y to f e e d in m i c r o h a b i t a t s
where
d i a t o m s are m o r e f r e q u e n t c a n n o t be
r u l e d out. T h e a b i l i t y to f e e d on f u n g a l
h y p h a e in c o n t r a s t to c. volutator h a s
already been mentioned.
Similarly,
Corophium volutator, b y
selecting
small particles,
t e n d s to
ingest a relatively
l a r g e r p o r t i o n of
bacteria.
The results also show that
a t t e m p t s to s t u d y t h e i n g e s t i o n r a t e
and the assimilation
efficiency
of
deposit-feeders
by measuring
the cont e n t s of o r g a n i c c a r b o n in t h e s u b s t r a t e
a n d in f a e c a l m a t e r i a l m a y b e u n r e a l i s t i c in s o m e cases.
In m o s t c a s e s , i n v e s t i g a t i o n s
on c o e x i s t i n g s p e c i e s a r e c a r r i e d o u t on
closely related forms which are fundamentally
identical
as r e g a r d s b e h a v ioural patterns and physiological
and
morphological
features,
all of w h i c h
change only slowly through evolution;
such coexisting
s p e c i e s m o s t l y s e e m to
differ along a single niche dimension,
often implying size differences,
and
t h u s the s i z e s of f o o d p a r t i c l e s
or
p r e y a n d m o s t c a s e s of c h a r a c t e r d i s placement
documented
in the l i t e r a t u r e
involve size differences
(Hutchinson,
1959; M a c A r t h u r ,
1972). S u c h c a s e s are
in o n e s e n s e m o r e e a s i l y a n a l y s e d . T h u s ,
as w i l l l a t e r be s h o w n ( F e n c h e l , in p r e p a r a t i o n ) , t h e t w o s p e c i e s of Hydrobia in
the locality studied exhibit differences
127
in t h e r a n g e of p a r t i c l e
sizes ingested
which can explain their coexistence.
When dealing with coexisting,
unrelated deposit-feeders,
w e m a y find,
in a d d i t i o n to p a r t i c l e
size-selection,
that they also differ in a number of
other niche dimensions
r e l a t e d to f o o d
selectivity.
T h u s , in t h e c a s e of Corophium volutator,
we have evidence that
this species can utilize suspended
food particles,
whereas hydrobiids
can
f e e d on p a r t i c l e s
a d h e r i n g to l a r g e r
surfaces and perhaps trap particles
on the s u r f a c e f i l m o f w a t e r w i t h m u c u s ;
there are also considerable
differences
in t h e i r b e h a v i o u r a l
patterns,
as e x e m p l i f i e d by t h e c h o i c e e x p e r i m e n t s .
I n d e e d , the a b i l i t y to u s e a l t e r n a t i v e
feeding mechanisms
s e e m s to be an att r i b u t e of m a n y d e p o s i t - f e e d i n g
animals.
Thus, evidence shows that the lugworm
Arenicola marina in a d d i t i o n to s w a l l o w i n g
s e d i m e n t m a y a l s o f u n c t i o n as a s u s p e n Nereis diversicolor f i l t e r s
sion feeder.
w a t e r w i t h a s e c r e t e d m u c u s bag, b u t
is a l s o k n o w n to be a p r e d a t o r ,
and not
infrequently
mineral particles
are f o u n d
in its g u t (for r e f e r e n c e s
and other
e x a m p l e s see N e w e l l ,
1970). T h u s , in
o r d e r to u n d e r s t a n d
the diversity
of
coexisting
deposit-feeders,
several
niche dimensions
besides particle
sizeselection must be considered.
These
mechanisms
w i l l l e a d to a p a r t i t i o n i n g
of t h e t o t a l r e s o u r c e s p e c t r u m o f s m a l l
food particles
a v a i l a b l e to d e p o s i t
feeders, although this resource partit i o n i n g is n o t as o b v i o u s as p r e y specificity
of p r e d a t o r s .
Acknowledgement. This study was in part
supported by grants from "Det Naturvidenskabelige Forskningsr~d".
Litdrature Cited
Fenchel, T.: The ecology of marine microbenthos
IV. Structure and function of the benthic
ecosystem, its chemical and physical factors
and the microfauna communities, with special reference to the ciliated protozoa.
Ophelia 6, 1-182 (1969)
- Studies on the decomposition of organic
detritus derived from the turtle grass
Thalassia testudinum. Limnol. Oceanogr. 15,
14-20 (1970)
- Aspects of decomposer food chains in marine
benthos. Verh. dt. zool. Ges. (65 Jahresvers.), 14-22 (1972)
Hargrave, B. : The utilization of benthic microflora by Hyalella azteca (amphipod). J.
Anim. Ecol. 39, 427-437 (1970)
Hutchinson, G.E.: Homage to Santa Rosalia or
why are there so many kinds of animals.
Am. Nat. 93, 145-159 (1959)
T. F e n c h e l et al. : P a r t i c l e
128
L.H.: The f e e d i n g b i o l o g y of Hydrobia
ventrosa I. The a s s i m i l a t i o n of d i f f e r e n t
Kofoed,
c o m p o n e n t s of the food. J. exp. mar. biol.
Ecol. (In press, a)
- The f e e d i n g b i o l o g y of Hydrobia ventrosa
II. The a l l o c a t i o n of the p a r a m e t e r s of the
carbon budget. J. exp. mar. biol. Ecol. (In
press, b)
Kohn, A.J.: D i v e r s i t y , u t i l i z a t i o n of resources,
and adaptive r a d i a t i o n in s h a l l o w - w a t e r
marine i n v e r t e b r a t e s of t r o p i c a l o c e a n i c
islands. Limnol. Oceanogr. 16, 332-348 (1971)
H y l l e b e r g Kristensen, J.: C a r b o h y d r a s e s of some
marine i n v e r t e b r a t e s with notes on t h e i r
food and on the n a t u r a l o c c u r r e n c e of the
c a r b o h y d r a t e s studied. Mar. Biol. 14,
130-142 (1972)
Levinton, J.: S t a b i l i t y and t r o p h i c s t r u c t u r e
in d e p o s i t - f e e d i n g and s u s p e n s i o n - f e e d i n g
communities. Am. Nat. 106, 472-486 (1972)
M a c A r t h u r , R.H.: G e o g r a p h i c a l ecology, 269 pp.
N e w York: H a r p e r & Row 1972
and R. Levins: C o m p e t i t i o n , h a b i t a t selection and c h a r a c t e r d i s p l a c e m e n t in a p a t c h y
e n v i r o n m e n t . Proc. natn. Acad. Sci. U.S.A.
51, 1207-1210 (1964)
Mangum, C.P. : Studies on s p e c i a t i o n in m a l d a n i d
p o l y c h a e t e s of the N o r t h A m e r i c a n A t l a n t i c
coast. II. D i s t r i b u t i o n and c o m p e t i t i v e
i n t e r a c t i o n of five s y m p a t r i c species.
Limnol. Oceanogr. 9, 12-26 (1964)
Date of final m a n u s c r i p t
acceptance:
J a n u a r y 20,
Size-Selection
of two D e p o s i t Feeders
Meadows, P.S.: E x p e r i m e n t s on substrate selection b y Corophium species: films and bact e r i a on sand particles. J. exp. Biol. 41,
499-511 (1964)
- and A. Reid: The b e h a v i o u r of Corophium
volutator (Crustacea: Amphipoda). J. Zool.,
Lond. 150, 387-399 (1966)
Muus, B.J.: The fauna of Danish e s t u a r i e s and
lagoons. D i s t r i b u t i o n and e c o l o g y of
d o m i n a t i n g species in the s h a l l o w b e a c h e s
of the m e s o h a l i n e zone. Kommn Danm. Fisk.og Havunders. (N.S.) 5, 1-316 (1967)
Newell, R.C.: The role of detritus in the
n u t r i t i o n of two marine d e p o s i t - f e e d e r s ,
the p r o s o b r a n c h Hydrobia ulvae and the
b i v a l v e Macoma balthica. Proc. zool. Soc.
Lond. 144, 25-45 (1965)
- B i o l o g y of i n t e r t i d a l animals, 555 pp. London: Logos Press Ltd. 1970
Reid, A.B. and A. Reid: F e e d i n g p r o c e s s e s of
m e m b e r s of the genus Macoma (Mollusca:
B i v a l v i a . Can. J. Zool. 47, 644-657 (1969)
Dr. Tom F e n c h e l
D e p a r t m e n t of E c o l o g y
U n i v e r s i t y of A a r h u s
D K - 8 0 0 0 ~rhus C
Denmark
1975. C o m m u n i c a t e d by T. Fenchel,
Arhus