in the inhalant (c i) and exhalant (c e) currents were estimated with an electronic particle counter. The clearance was calculated as Y = FI(I _~e), where F1 flow.
Marine Biology 54, 143-147 (1979)
MARINE BIOLOGY 9 by Springer-Verlag 1979
Filtration Rate, Using a New Indirect Technique, in Thirteen Species of Suspension-Feeding Bivalves F. M~hlenberg and H.U. Riisg~rd Marine Pollution Laboratory, National Agency of Environmental Protection; Kavalerg~,rden6, DK-2920 Charlottenlund, Denmark
Abstract
A m e t h o d for d e t e r m i n i n g f i l t r a t i o n rates in u n d i s t u r b e d s u s p e n s i o n - f e e d i n g biv a l v e s is d e s c r i b e d . C o n c e n t r a t i o n s of p a r t i c u l a t e m a t t e r in the w a t e r c o l l e c t e d in the i n h a l a n t (ci) and e x h a l a n t (ce) c u r r e n t s w e r e e s t i m a t e d w i t h an e l e c t r o n i c particle
counter.
The
c l e a r a n c e was
calculated
as Y = FI(I _~e),
where
F1
flow
rate t h r o u g h the tube c o l l e c t i n g e x h a l a n t water. Only above c r i t i c a l levels of water flow (FI) w e r e c l e a r a n c e s r e p r e s e n t a t i v e of f i l t r a t i o n rates. At 10 ~ to 13oc, the f i l t r a t i o n r a t e s (F, 1 h-l) w i t h i n one or two o r d e r s of m a g n i t u d e of dry w e i g h t (w, g) , in Cardium echinatum L. , C. edule L. , Mytilus edulis L. , Modiolus modiolus (L.) and Arctica islandica (L.) f o l l o w e d the a l l o m e t r i c e q u a t i o n s : 4.22w0.62, 11.60wO.70, 7 . 4 5 w O . 6 6 , 6 . O O w O'75 and 5 . 5 5 w 0-62, r e s p e c t i v e l y . Five s p e c i e s of biv a l v e s [ Spisula subtruncata (da Costa) , Hiatella striata (Fleuriau) , Cultellus pellucidus (Pennant), Mya arenaria L. and venerupis pullastra (Montagu) ] f i l t e r e d w i t h the same rates as i n d i v i d u a l s of Cardium echinatum and A. islandica of e q u i v a l e n t soft weight. In Pecten furtivus and P. opercularis f i l t r a t i o n rates w e r e about twice the rates m e a sured in i n d i v i d u a l s of Mytilus edulis of c o m p a r a b l e b o d y weight. The g i l l area in M. edulis i n c r e a s e s w i t h size at the same rate as the f i l t r a t i o n rate.
I ntroduction
The l i t e r a t u r e cites m a n y d e t e r m i n a t i o n s of f i l t r a t i o n rates in s u s p e n s i o n - f e e d ing b i v a l v e s , but u n f o r t u n a t e l y r e s u l t s are often d i f f i c u l t to c o m p a r e b e c a u s e of the d i f f e r e n t e x p e r i m e n t a l c o n d i t i o n s used. This is c o n s p i c u o u s in the m u s s e l Mytilus edulis, w h e r e the rates of w a t e r t r a n s p o r t r e c o r d e d by d i f f e r e n t a u t h o r s v a r y by as m u c h as ten times (J~rgensen, 1975, his Fig. I, and W i n t e r , 1978, his T a b l e I). It is p o s s i b l e to p o i n t out some of the m a i n r e a s o n s for t h e s e disc r e p a n c i e s : (a) b i v a l v e s are v e r y sensitive to m e c h a n i c a l or c h e m i c a l d i s t u r b a n c e s (J~rgensen, 1960); (b) m o s t meas u r e m e n t s on i n f a u n a l b i v a l v e s have been m a d e on i n d i v i d u a l s o u t s i d e t h e i r n o r m a l substrate; (c) finally, in f l o w - t h r o u g h systems, r e c i r c u l a t i o n of e x h a l e d w a t e r a r o u n d e x p e r i m e n t a l b i v a l v e s can cause u n d e r e s t i m a t e s of f i l t r a t i o n rate (Hildreth and Crisp, ]976; R i i s g & r d , 7977). This r e p o r t p r e s e n t s a n e w i n d i r e c t m e t h o d of f i l t r a t i o n - r a t e e s t i m a t i o n
w h i c h e n s u r e s that r e c i r c u l a t i o n of exh a l e d w a t e r is n e g l i g i b l e . The m e t h o d is u s e d to e s t i m a t e f i l t r a t i o n rates in und i s t u r b e d i n d i v i d u a l s of 13 s p e c i e s of e p i f a u n a l and i n f a u n a l b i v a l v e s .
Materials and Methods
The e x p e r i m e n t s w e r e m a d e at the M a r i n e B i o l o g i c a l L a b o r a t o r y , H e l s i n g ~ r , Denmark, from A p r i l to O c t o b e r , 1978. S p e c i m e n s of Cardium echinatum L., C. edule L. , Mytilus edulis L. , Modiolus modiolus (L.) , Arctica islandica (L.) , Spisula subtruncata (da Costa), Hiatella striata (Fleuriau) , Cultellus pellucidus (Pennant , Musculus niger (Gray), Mya arenaria L . , Pecten furtivus M ~ l l e r and p. opercularis (L.)
w e r e c o l l e c t e d in the n o r t h e r n part of ~resund, D e n m a r k , w h i l e venerupis pullastra (Montagu) came from W e s e r E s t u a r y , FRG. B i v a l v e s w e r e k e p t in the l a b o r a t o r y s e a - w a t e r system. E x p e r i m e n t a l t e m p e r a tures r a n g e d f r o m 10 ~ to 13oc and salinity was about 30%.
0025-3162/79/0054/0143/S01.00
144
F. M~hlenberg and H.U. Riisg~rd: Filtration Rates in Bivalves
E p i f a u n a l b i v a l v e s s o o n e m b y s s e d in the acclimation aquaria, while the inf a u n a l b i v a l v e s b u r i e d t h e m s e l v e s in sediment-containing beakers. Bivalves w e r e f e d m i x e d a l g a l c u l t u r e s at l e a s t twice a week. In order to minimize dist u r b a n c e , e x p e r i m e n t s w e r e p e r f o r m e d in t h e a c c l i m a t i o n a q u a r i a o f 10 to 30 1 volume. To estimate filtration rate, samples of i n h a l e d a n d e x h a l e d w a t e r w e r e siphoned through glass tubes placed above the bivalve's inhalant and exhalant apertures, respectively (see M ~ h l e n b e r g and Riisg&rd, ]978, t h e i r Fig. 2). T h e s i p h o n a l f l o w r a t e w a s v a r i e d f r o m 5 to 1500 ml min-1, using clamping screws and d i f f e r e n t d i a m e t e r s of g l a s s t u b e s . T h e tube collecting the exhaled water had a f i t t i n g w h i c h w a s s i m i l a r in f o r m to, b u t at l e a s t f i v e t i m e s l a r g e r t h a n , t h e bivalve's exhalant aperture. The two t u b e s w e r e i d e n t i c a l in a l l o t h e r r e spects.
T h e v o l u m e of c o l l e c t e d e x h a l e d w a t e r c l e a r e d of p a r t i c l e s p e r u n i t o f t i m e ( c l e a r a n c e = Y, m l m i n - 1 ) w a s c a l c u lated
as"
ce
Y = FI(I-c--7) , w h e r e
is t h e
F1
flow rate through the glass siphons (ml rain-]), a n d c i a n d ce a r e t h e c o n c e n t r a t i o n s of a l g a l c e l l s in t h e w a t e r simultaneously c o l l e c t e d in t h e i n h a l a n t a n d e x h a l a n t c u r r e n t s , r e s p e c t i v e l y , ci and ce were determined by a Coulter Counter, Model TAII. T h e f l o w r a t e s in the two tubes were kept equal, and measured by collecting the water over a timed period. The time-period over which filtration was measured varied between 30 rain a n d 2 h. Clearances measured represent only the true filtration rates at high flow r a t e s (El); h e r e t h e c l e a r a n c e v a l u e s b e c o m e i n d e p e n d e n t o f f l o w r a t e . Fig. I shows that recirculation of exhaled water was negligible at t h e f l o w r a t e s
500
500
Y=FI c •
X
# x
."
E
w 10(
Y=FI
ua I0C
U
Q
U
o
n~
o~
8 < UJ ~
< IJA ~
50 9
-
9
50
~o
I000
IOO FLOW RATE (FU m i l m n
I0
I00
I000 FLOW RATE (FI), m[/min
500-
E
Y=FI
uJ tOO < w,
6
50
9
9
,
10
mn 100
,
,
,
,
FLOW RATE (Fl),mi/min
,
,,
1000
Fig. i. Clearance (Y) as a function of flow rate (El) for bivalves of various dry weights. Lines for clearance = flow rate (Y = FI) are shown. Each plateau represents true filtration rate. (A) M o d i o l u s m o d i o lus: triangles, 42 mg; filled circles, 281 mg; open circles, 627 mg; crosses, 1555 mg. (B) C a r d i u m e c h i n a t u m : filled circles, 126 mg; triangles, 579 mg; crosses, 744 mg; open circles, 1814 mg. (C) A r c t i c a i s l a n d i c a : crosses, 72 mg; open circles, 222 mg; filled circles, 310 mg; triangles, 1310 mg
F. M~hlenberg and H.U. Riisg~rd: Filtration Rates in Bivalves
u s e d to e s t i m a t e f i l t r a t i o n rate in this study. The u n i c e l l u l a r a l g a e Phaeodactylum tricornutum, Dunaliella marina and Tetraselmis suesica w e r e u s e d as food and for m e a s u r e m e n t s of f i l t r a t i o n rates, since und i s t u r b e d b i v a l v e s r e t a i n these algae c o m p l e t e l y (M~hlenberg and R i i s g ~ r d , 1978). P r i o r to e a c h e x p e r i m e n t , the s e a - w a t e r flow t h r o u g h the a q u a r i u m was s t o p p e d and algal c u l t u r e s w e r e a d d e d to give i n i t i a l c o n c e n t r a t i o n s of b e t w e e n 2,000 and 10,000 cell ml-1. M e a s u r e m e n t s w e r e m a d e o n l y on u n d i s t u r b e d b i v a l v e s w h e n t h e i r a p e r t u r e s or s i p h o n s w e r e judged to be fully o p e n and e x t e n d e d . To m e a s u r e the area of the gills, mgtilus edulis w i t h one v a l v e r e m o v e d w e r e p l a c e d on one side, immersed, and p h o t o graphed. The gill a r e a was e s t i m a t e d f r o m the w e i g h t of the p h o t o g r a p h of the o u t e r d e m i b r a n c h . The t o t a l area c o u l d be o b t a i n e d by m u l t i p l i c a t i o n by 8, since the 4 d e m i b r a n e h s are about the same size. A f t e r the e x p e r i m e n t s , shell length and d r y w e i g h t of the soft p a r t s w e r e determined.
145
in the n o r t h e r n p a r t of ~ r e s u n d (Dr. W. N i c o l a i s e n , p e r s o n a l c o m m u n i c a t i o n ) and were p r o b a b l y b e l o w c o n c e n t r a t i o n s w h i c h m a y r e d u c e f i l t r a t i o n rates (see Winter, 1973; J ~ r g e n s e n , 1975). The b i v a l v e s n e v e r p r o d u c e d p s e u d o f a e c e s d u r i n g the experiments. In m o s t of the b i v a l v e species, high f i l t r a t i o n rates w e r e o b s e r v e d w i t h i n 30 m i n a f t e r algal addition. If no addit i o n a l a l g a e were added, the f i l t r a t i o n rate g r a d u a l l y fell c o n c u r r e n t l y w i t h the d e p l e t i o n of s u s p e n d e d algae. O n l y in Cardium edule and in the p e c t i n i d s w e r e the f i l t r a t i o n rates a l w a y s h i g h and ind e p e n d e n t of algal addition. High f i l t r a t i o n rates were c o r r e l a t e d w i t h fully o p e n v a l v e s and e x t e n d e d s i p h o n s or m a n t l e edges, d e c r e a s i n g f i l t r a t i o n rates w i t h p a r t i a l c l o s u r e of the valves, siphons, or m a n t l e edges. The f i l t r a t i o n rates (F, 1 h-l) in the b i v a l v e s w e r e h i g h l y c o r r e l a t e d w i t h dry w e i g h t of the soft t i s s u e s (w, g). Fig. 2 and T a b l e I show that the filtration rate (F) in Cardium echinatum, C. edule, Mytilus edulis, Modiolus modiolus and Arctica islandica i n c r e a s e s w i t h increasing body w e i g h t (w) a c c o r d i n g to the e q u a t i o n F = a W b. The b - v a l u e s b e t w e e n 0.62 and 0.75 found in this study a g r e e w i t h t h o s e of R i i s g ~ r d and M ~ h l e n b e r g (1979) and the a u t h o r s listed by W i n t e r (1978, his Table I). In Mytilus edulis, the b - v a l u e was the same as the e x p o n e n t 0.66 of the
Results
The c o n c e n t r a t i o n s of p a r t i c u l a t e m a t t e r u s e d (0.02 to 0 . 3 0 mg dry w e i g h t o r g a n i c m a t t e r 1-I) fell w i t h i n the n o r m a l r a n g e
v v
c
D v
E
A
LU
J
F o
001
/
(~
/
i
i
i
,
i
i ~ pl 0.1 DRY
~ WEIGHT
OF
J
i
TISSUES
i
i
i i t 1,D
L
f
(W),g
Fig. 2. Filtration rate (F) as a function of flesh weight (W) in various bivalves. Regression lines are shown for Cardium echinatum (A), C. edule (B), Mytilus edulis (C), Modiolus modiolus (D] and Arctica islandica (E). Open circles: Spisula subtruncata; filled circle: Hiatella striata; open triangles: Cultellus pellucidus; Filled triangle: Musculus niger; crosses: Mya arenaria; open square: Venerupis pullastra; filled square: Pecten furtivus; inverted triangles: Pecten opercularis
.
148
.
o
F. M~hlenberg and H.U. Rlmsgard: Filtration Rates in Bivalves
T a b l e I. R e g r e s s i o n constants of filtration r a t e (F, 1 h-l) a n d g i l l a r e a (G, cm 2) o n d r y f l e s h w e i g h t (W, g) in v a r i o u s b i v a l v e s , n : number of individuals and r = correlation coefficient. Regression equat i o n s : F o r G = a W b. SE: s t a n d a r d error Species
Regression
n
W
Cardium echinatum
F on W
io
a ~ SE
b ~ SE
.08o-2.13o 4.22~i.o5 .62s
r
.99
Cardium edule
F on W
9
.o28-o.173 Ii.60~1.27 .70~.09 .95
Mytilus edulis
F on W
6
.O11-1.361
7.45~.13
.66~.O4 .99
Modiolus m o d i o l u s
F on
7
.058-1.555
6.00•
.75s
.98
Arctica islandica
F on W
7
.011-i.310 5.55s
.62s
.99
Mytilus edulis
G on
W
W
28
g i l l area, e x p r e s s e d as a f u n c t i o n of b o d y s i z e (Table I). A n a l y s i s of c o v a r i a n c e s h o w e d t h a t t h e e x p o n e n t s of a l l regression lines were not significantly different f r o m o n e a n o t h e r at P = 0.05. A few observations indicate that weightspecific filtration r a t e s in Spisula subtruncata, Hiatella striata, Cultellus pellucidus, Mya arenaria a n d Venerupis pullastra a r e s i m i l a r to v a l u e s d e s c r i b e d in T a b l e I (see Fig. 2). H o w e v e r , Pecten furtivus a n d p. opercularis s h o w e d m u c h h i g h e r f i l t r a t i o n r a t e s , w h i l e t h e s i n g l e Musculus niger (0.300 g d r y w e i g h t ) filtered only O. 48 1 h-1.
Discussion
Several workers have published extensive r e c o r d s of t h e f i l t r a t i o n r a t e s of Mytilus edulis, as r e v i e w e d b y F o s t e r - S m i t h (1975) a n d W i n t e r (1978). T h e r a t e s m e a s u r e d in t h i s s t u d y a r e c o n s i d e r a b l y higher than most filtration rates previously reported, but agree with those we d e t e r m i n e d b y a n o t h e r t e c h n i q u e (Riisgard and M~hlenberg, 1979). In g e n e r a l , the r a t e s m e a s u r e d in t h i s work are higher than the filtration rates previously reported. This applies to Cardium edule, Modiolus modiolus a n d Arctica islandica, t h e w a t e r t r a n s p o r t c a p a c i t i e s of w h i c h w e h a v e f o u n d to b e 3 to 6 times higher than previously measured f i l t r a t i o n r a t e s (see W i n t e r , 1978, h i s T a b l e 1). In Pecten opercularis, w e o b tained filtration rates only slightly h i g h e r t h a n t h o s e r e c o r d e d by V a h l (1972) for t h i s s p e c i e s . T h e p o s s i b l e m a i n r e a s o n s for t h e d i s c r e p a n c i e s have a l r e a d y b e e n p o i n t e d o u t in t h e " I n t r o duction" ( m e c h a n i c a l or c h e m i c a l d i s t u r bances, measurements on i n f a u n a l b i valves outside their natural substrate, recirculation), and other experimental conditions, e.g. a b n o r m a l l y h i g h a l g a l concentrations and bad water quality may r e s u l t in p a r t i a l c l o s u r e of the v a l v e s
.010-0.860 24.58~O.O5 .66~.O5 .93
and subsequently reduced filtration r a t e s (see R i i s g [ r d a n d M @ h l e n b e r g , 1979). P u b l i s h e d v a l u e s of f i l t r a t i o n r a t e s for epifaunal species are generally higher than for infaunal species. J~rgensen (1966) w a s u n c e r t a i n w h e t h e r l o w f i l t r a t i o n r a t e s a r e t y p i c a l for i n f a u n a l b i v a l v e s or w h e t h e r l o w f i l t r a t i o n r a t e s w e r e d u e to the e x p e r i m e n t s being performed on infaunal bivalves kept away from their natural substrate (Rice a n d S m i t h , 1958; H e r s h , 1960; A l l e n , 1962; W i n t e r , 1969). C o n s i d e r i n g our results, the l a t t e r e x p l a n a t i o n appears most probable. T h e a u t h o r s o b s e r v e d in t h e s u m m e r of 1978, d u r i n g d i v e s in a b r a c k i s h - w a t e r a r e a ( L i m f j o r d e n , D e n m a r k ) t h a t in s e v eral localities with good water exchange a l l Cardium edule, Mytilus edulis, Mya arenaria a n d Venerupis pullastra, w e r e w i d e o p e n , a n d m a n y of t h e m h a d a h e a v y f a e c e s p r o duction. This contrasted with the situat i o n in l o c a l i t i e s w i t h p o o r w a t e r e x c h a n g e , w h e r e Mytilus edulis w a s m o r e or less c l o s e d . It w o u l d be of i n t e r e s t to k n o w to what extent the water-transport capacities measured in t h e p r e s e n t w o r k a r e e x p l o i t e d in n a t u r e . T h e h i g h s e n s i t i v ity of b i v a l v e s to l a b o r a t o r y c o n d i t i o n s and our observations in n a t u r e i n d i c a t e that this exploitation is e a s i l y i n f l u enced by environmental factors.
Acknowledgements. Thanks are due to Mr. P. Sand Kristensen for supplying the algal cultures, and to Dr. K.W. Ockelmann for verifying the names of the bivalves and for help in other ways. We are also very grateful to the Marine Biological Laboratory, Helsing~r, for provision of facilities, and to Miss A. Claudius Nielsen for technical assistance. Finally, we would like to thank Professor C. Barker J~rgensen for many fruitful discussions and for his criticism of the manuscript.
F. M~hlenberg
9
.
o
and H.U. Rl~sgard:
Filtration Rates in Bivalves
Literature Cited Allen, J.A.: Preliminary experiments on the feeding and excretion of bivalves using Phaeodactylum labelled with 32p. j. mar. biol. Ass. U.K. 42, 609-623 (1962) Foster-Smith, R.L.: The effect of concentration of suspension on the filtration rates and pseudofaecal production for Mytilus edulis L., Cerastoderma edula (L.) and Venerupis pullastra (Montagu). J. exp. mar. Biol. Ecol. 17, 1-22 (1975) Hersh, G.L.: A method for the study of the water currents of invertebrate ciliary filter feeders. Veliger 2, 77-83 (1960) Hildreth, D.I. and D.J. Crisp: A corrected formula for calculation of filtration rate of bivalve molluscs in an experimental flowing system. J. mar. biol. Ass. U.K. 56, 111-120 (1976) J~rgensen, C.B.: Efficiency of particle retention and rate of water transport in undisturbed lamellibranchs. J. Cons. perm. int. Explor. Mer 26, 94-116 (1960) Biology of suspension feeding, 645 pp. New York: Academic Press 1966 - Comparative physiology of suspension feeding. A. Rev. Physiol. 37, 57-79 (1975) M~hlenberg, F. and H.U. Riisg[rd: Efficiency of particle retention in 13 species of suspen-
Date of final manuscript
acceptance:
June 22,
147
sion feeding bivalves. Ophelia 17, 239-246 (1978) Rice, T.R. and R.J. Smith: Filtering rates of the hard clam (Venus mercenaria) determined with radioactive phytoplankton. Fishery Bull. Fish Wildl. Serv. U.S. 58, 73-82 (1958) Rllsgard, H.U.: On measurements of the filtration rates of suspension feeding bivalves in a flow system. Ophelia 16, 167-173 (1977) and F. M~hlenberg: An improved automatic recording apparatus for determining the filtration rate in Mytilus edulis as a function of size and algal concentration. Mar. Biol. 52, 61-67 (1979) Vahl, 0.: Particle retention and relation between water transport and oxygen uptake in Chlamys opercularis (L.) (Bivalvia). Ophelia 10, 67-74 (1972) Winter, J.E.: Uber den EinfluB der Nahrungskonzentration und anderer Faktoren auf Filtrierleistung und Nahrungsausnutzung der Muscheln Arctica islandica und Modiolus modiolus. Mar. Biol. 4, 87-135 (1969) - The filtration rate of Mytilus edulis and its dependence on algal concentration, measured by a continuous automatic apparatus. Mar. Biol. 22, 317-328 (1973) A review on the knowledge of suspension-feeding in lamellibranchiate bivalves, with special reference to artificial aquaculture systems. Aquaculture 13, 1-33 (1978) .
.
o
-
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1979. Communicated by T.M. Fenchel,
Aarhus
