Accumulation of cadmium by abarenicola pacifica

T h e Science o f t h e Total E n v i r o n m e n t , 28 (1983) 1 0 5 - - 1 1 8 Elsevier Science Publishers B.V., A m s t e r d a m - - Printed in The Netherlands

105

ACCUMULATION OF CADMIUMBY ABARENICOLA PAClFICA STEWART M. OAKLEY, KENNETH J. WILLIAMSON, and PETER O. NELSON C i v i l Engineering Department, Oregon State U n i v e r s i t y , C o r v a l l i s , Oregon

ABSTRACT The b i o a v a i l a b i l i t y

of trace metals to marine organisms depends on trace metal

p a r t i t i o n i n g among geochemical phases and on the k i n e t i c s of uptake from each phase.

This study was undertaken to develop a k i n e t i c model f o r trace metal

uptake based on e q u i l i b r i u m p a r t i t i o n i n g of the metal in aqueous and sedimentary phases. A three compartment model was developed and used to estimate the accumulation of cadmium under short term laboratory conditions.

The rate of cadmium uptake

from bentonite c l a y , humic acid, f e r r i c hydroxide, and seawater was measured f o r the deposit-feeding polychaete Abarenicola p a c i f i c a . The r e s u l t s show t h a t , under the conditions of t h i s study, bentonite clay and ferric

hydroxide can be more important sources of cadmium than seawater f o r

Abarenicola p a c i f i c a .

INTRODUCTION Marine and estuarine organisms are known to accumulate high levels of trace metals in t h e i r tissues [ I ] .

Both Bowen [2] and Polikarpov [3] have stated that

marine animals s a t i s f y needs f o r required metals by d i r e c t absorption from the surrounding water, and most e a r l y studies on trace metal uptake have assumed that uptake mainly occurred from s o l u t i o n [ 4 - 6 ] .

Other evidence, however, supports

the view that some marine organisms absorb trace metals c h i e f l y from food [ 7 , 8 ] . This f a c t suggests that a s i g n i f i c a n t uptake of trace metals may occur in those organisms which depend on sediment as a food source since trace metal concentrations in aquatic sediments are t y p i c a l l y orders of magnitude higher than concent r a t i o n s in the water column. Several i n v e s t i g a t o r s have conducted laboratory studies to assess the accumul a t i o n of sediment-bound metals to benthic organisms [9-14].

The r e s u l t s of

Luoma and Jenne [11,12] suggested that sediment-bound metals can be r e a d i l y bioaccumulated depending on the p a r t i c u l a r geochemical phase with which a metal is associated, while the r e s u l t s of Renfro [ 9 ] , Ueda et al [ I 0 ] , 0048-9697/83/$03.00

© 1983 Elsevier Science Publishers B.V.

Neff et al [ 1 3 ] , and

106 Ray et al LI4] were e i t h e r i n c o n c l u s i v e , or showed uptake from sediments to be n e g l i g i b l e as compared to water. I t was the objective of t h i s research to determine whether uptake of trace metals may be important to benthic organisms that ingest sediments as food. Cadmium was chosen as the metal of i n t e r e s t due to i t s known t o x i c i t y to organisms and i t s p o t e n t i a l health effects i f bioaccumulated through marine food chains. EXPERIMENTAL DESIGN Experiments to determine the r e l a t i v e uptake of metals by benthic organisms from sediments, food and/or water are d i f f i c u l t number of v a r i a b l e s .

The various d i f f i c u l t i e s

oesign chosen to minimize the d i f f i c u l t i e s

to conduct due to the large that must be avoided and the

are l i s t e d below.

F i r s t , accumulation from the sediments depends upon the p a r t i c u l a r geochemical phase with which the metal is associated [11,12].

As a r e s u l t , accumu-

l a t i o n from spiked natural sediments having unknown metal d i s t r i b u t i o n s among the various phases are d i f f i c u l t

to extrapolate to varying conditions.

In a d d i t i o n ,

portions of metals in natural sediments are not b i o a v a i l a b l e , and no methods have been developed to accurately estimate these nonavailable portions [ I I ] . these d i f f i c u l t i e s ,

single geochemical phases of sand, clays, f e r r i c

To avoid

hydroxide,

and humic acid were used instead of natural sediments f o r a l l experiments. four phases are the known major components of marine sediments.

These

The associations

of metals with these phases are known to be dominated by adsorption which can be modelled by adsorption isotherms LI5].

At environmental concentrations of i n t e r e s t ,

these isotherms are l i n e a r f o r cadmium and the adsorption is r e v e r s i b l e which insures t o t a l p o t e n t i a l b i o a v a i l a b i l i t y .

This experimental approach is e s p e c i a l l y

useful since i t has been shown that metal adsorption in natural sediments can be accurately estimated as the l i n e a r sum of the adsorption to the i n d i v i d u a l geochemical phases LI6]. Second, a true deposit-feeding organism that ingests a l l sediment phases nee6s to be chosen since sediments are added as mixtures of phases. gators [ I 0 , I I , 1 3 , 1 4 ]

Several i n v e s t i -

have used organisms that are s e l e c t i v e feeders f o r c e r t a i n

portions of the sediment and/or the surface layer.

The r e s u l t s of these studies

are inconclusive when applied to bulk sediment concentrations of metals.

For our

studies, the deposit-feeding polychaete worm, Abarenicola p a c i f i c a was chosen since i t is known to pass large q u a n t i t i e s of sediment through i t s gut, and e a s i l y adapts to experimental conditions [17-21].

A. p a c i f i c a occupies a U-shaped

burrow consisting of a s a n d - f i l l e d head-shaft and an open t a i l - s h a f t ; u s u a l l y occupies the h o r i z o n t a l portion of the U-tube.

the worm

A. p a c i f i c a feeds by

taking in sediment at the base of the head-shaft and excreting feces at the opening of the t a i l - s h a f t . T h i r d , the uptake of metals from food needs to be held constant or minimized.

107 The d i e t a r y organics f o r benthic organisms w i l l phase and metals w i l l

act as an a d d i t i o n a l sediment

be p a r t i t i o n e d i n t o t h i s phase.

the b i o t i c and a b i o t i c phases w i l l

likely

n i t r o g e n and c a l o r i c contents [ 2 2 - 2 4 ] .

The feeding rates of both

depend upon the food type, and the

This adds serious complications in i n t e r -

p r e t i n g r e s u l t s , and f o r t h i s reason, we chose to conduct the experiments w i t h starved organisms.

I t was assumed t h a t the organisms maintained a constant res-

p i r a t i o n r a t e , a maximum i n g e s t i o n r a t e of the a r t i f i c i a l n e a r l y constant body weights over the t e s t i n g p e r i o d .

sediment phases, and

( h i s is supported by Kay

and B r a f i e l d [25] who reported t h a t the polychaete Neanthes v i r e n underwent a weight loss of only 1.3% per day under s t a r v a t i o n and y e t maintained r e s p i r a t i o n rates equal to t h a t of fed c o n d i t i o n s . MATHEMATICAL MODEL The a v a i l a b l e evidence f o r the process of t r a c e metal a b s o r p t i o n and depuratio~ by an organism (whether from food, sediment, or water) suggests t h a t i t can be approximated by a f i r s t - o r d e r

compartment model [26-31].

For our c o n d i t i o n s of

starved organisms, a three-compartment model was used to describe the k i n e t i c s of accumulation from water and sediments (Fig. I ) as: d(C Mo) dt - kwCwVw + ksCsMs - D M°

(I)

d(CwVw) d~ - lw - low - kwCwVw

(2)

d(CsM s) dt - Is - los - ksCsMs

(3)

where: Iw

= metal i n p u t r a t e associated w i t h r e s p i r a t i o n ,

Cw

= metal c o n c e n t r a t i o n in water, ug/L

ug/d

Vw

= volume o f water in contact w i t h organism, L

low

= r a t e of unabsorbed metal e l i m i n a t i o n from water, ug/d

kw

= r a t e constant f o r metal absorption from water, I / L

C

= c o n c e n t r a t i o n o f metal in organism, ~g/g

Mo

= mass o f organism, g

Is

= metal i n p u t r a t e associated w i t h i n g e s t i o n , ug/d

Cs

= c o n c e n t r a t i o n o f metal in sediment, ug/g

Ms

= mass of sediment in g u t , g

los

= r a t e o f unabsorbed metal e l i m i n a t i o n from g u t , ug/d

ks

= r a t e constant f o r metal absorption from g u t , I / d

D

= depuration f u n c t i o n , ug/g-d

108 Cv Vw

Tow

Mefo from wa er kwCwV w r

C ,t 0

DM o

Met =1 in

org( nism ksCsM s

CsMs

~.,~,o,.om g

los

Metol

Fig. I . Three compartment model f o r the a d s o r p t i o n of trace metals from sediment and water by organisms.

I t is assumed t h a t the metal uptake from water in the gut is n e g l i b i b l e r e l a t i v e to t h a t from the sediment due to the small C

W

in r e l a t i o n to C and the small V S

W

in r e l a t i o n to Ms . Depuration is assumed to occur from more than one body component [32] and the depuration rates are expressed as net r a t e s .

As such, the depuration r a t e f o r

the gut would i n c l u d e e x c r e t i o n and subsequent r e a d s o r p t i o n . The depuration f u n c t i o n is formulated as: (4)

D : ke(i)C f o r Ci!CsCi+ 1 w i t h C = Co(i) at t=O where Ke(i)

= e l i m i n a t i o n constant f o r i th compartment, I / d

Co(i)

= initial

Ci,Ci+ 1

c o n c e n t r a t i o n in i th compartment, l~g/g, and

= lower and upper boundary l i m i t s ,

r e s p e c t i v e l y , ug/g.

I f the mass of the organism, Mo, is constant, Eq. 1 becomes: dC

C d~ = k* WW

(5)

+ k*S Cs - ke(i)C..

where k*= w

kV ww M 0

(6)

'

and

k~ =

ksMs M

(7)

0

Assuming t h a t C and C are constants, the p a r t i c u l a r W S becomes:

s o l u t i o n to Eq. 5

109

C=

k*w Cw + k*s Cs -ke(i)t -ke(i)t ke(i ) [l-e ] + Co(i)e

where C = Co(i) at t = O. of the i n i t i a l

(s)

The l a s t term in Eq. 8 accounts f o r the depuration

metal concentration Co(i).

I f there are several d i f f e r e n t geochemical phases, j ,

on which a metal is

p a r t i t i o n e d , Eq. 8 then becomes:

J k* C + Z k~(J)Cs(J) -ke(i)t -k ( i ) t C = w w keli~kl [l-e ] + Co(i)e e where Cs(J) = ~jCp(j) ~j

(9)

(I0)

and

is the f r a c t i o n of phase j in the t o t a l sediment on a weight basis, and Cp(j)

is the concentration of metal adsorbed on phase j .

Thus the r e l a t i v e importance

of uptake from water or sediment w i l l depend on the numerical values of k* Cw W

and j~ k~(j) Cs(J). There are several l i m i t a t i o n s on the use of t h i s model which must be recognized to avoid m i s i n t e r p r e t a t i o n of r e s u l t s • Although the rate constants k~, k*S ' and ke(i) are treated as constants in Eq. I , they are in r e a l i t y functions of th~ environmental conditions ( p h y s i c a l , chemical, b i o l o g i c a l ) under which the experiment was performed. i n d i v i d u a l organism•

In a d d i t i o n , the model is t h e o r e t i c a l l y v a l i d f o r only one Since i t is u s u a l l y necessary to s a c r i f i c e animals over

time, the v a r i a t i o n between d i f f e r e n t i n d i v i d u a l s of the same species w i l l duce large errors in parameter estimations.

intro-

At present, there are few population

models developed which can adequately account f o r the variance between i n d i v i d u a l s [33]. Despite these l i m i t a t i o n s , t h i s model can be used to give a f i r s t

approxima-

t i o n of the r e l a t i v e importance of water and d i f f e r e n t sediment phases in the accumulation of trace metals. METHODS Reagents and Glassware A l l laboratory glassware used were washed with 50% n i t r i c twice with d o u b l e - d i s t i l l e d water.

acid and rinsed

Polyethylene bottles were used f o r the s t o r -

age of a l l l i q u i d s o l u t i o n s . Acid-washed i g n i t e d sand ( j . T . artificial

Baker) that served as support material in the

sediments was used without modification•

Adsorption or p a r t i t i o n i n g

of trace metals onto the sand phase was found to be n e g l i g i b l e .

iio

Seawater ( s a l i n i t y - 32 °/oo) was collected from Oregon coastal waters, f i l t e r . ed s e q u e n t i a l l y through a sand f i l t e r

and 0.2 um membrane f i l t e r

( U l t i p o r ) , and

stored at 4°C in polyethylene b o t t l e s . Preparation of A r t i f i c i a l Sediments Bentonite clay, amorphous iron oxide (Fe(OH)3) and humic were prepared according to the procedures outlined previously [15].

Surface areas of the clay and

iron solids were approximately 32 m2/g, and 300 m2/g, respectively.

Solid phases

were dosed with Cd in seawater to give typical solid phase concentrations l i k e l y to be encountered in the natural environment; these concentrations were estimated by using the linear portion of adsorption isotherms as shown in Fig. 2 (the f u l l isotherms are shown in Oakley et al, 1981). The dosed solid phase was separated from the seawater medium by centrifugation, and then mixed with the acid-washed ignited sand. The f i n a l metal and solid phase concentrations used are l i s t e d in Table I. Before each experiment the requisite metal-phase-sand mixture (= 2000 g) was equilibrated in a polyethylene aquarium with 20 L of seawater for at least 24 hr. Sediment and solute metal concentrations were then monitored throughout the course of the experiment. A requisite volume of stock metal solution was added d i r e c t l y to the aquarium in the experiments monitoring uptake from seawater to give a total soluble metal concentration of 50 ~g/L for Cd.

Additional metal additions or pH adjustments

were not required.

300

I

'

l

,

i

I

t

,

t

,

25O

t

,

S-32%o

(OH)

PV-g°c

2OO

.? 150 ioo ntonite

50

o~

20

40

,

I

60

i

I

80

t

I

I00

i

I

120

i

I

140

t

160

[Cd]eq T, P-g/[

Fig. 2. Linear adsorption isotherms for Cd on bentonite, Fe(OH)3, and humic acid in seawater.

i11

TABLE 1 Concentrations of Cd in s o l i d and aqueous phases

So l i d phase

Cd concentration on pure s o l i d phase, Cp(j), ug/g

Bentonite Fe(OH) 3 Humic Acid Sand

Equilibrium aqueous Cd concentration ~g/L

8 22 0.8 .40

Fraction of s o l i d phase in t o t a l sediment, ~j

7.2 5.0 3.4 3.4-7.2

Cd concentration in t o t a l sediment Cs(J) , ug/g

0.5 0.039 1.0 0-0.96

3.8 3.4 0.8 0.8-3.8

Accumulation experiments Specimens of Abarenicola p a c i f i c a were c o l l e c t e d from the i n t e r t i d a l zone of Yaquina Bay, Oregon. heterogeneity.

A l l animals were c o l l e c ted from the same locale to minimize

The polychaetes were acclimated without feeding in f i l t e r e d sea-

water at 12°C f o r 24 hr p r i o r to each experiment.

Since metal accumulation w i l l

vary s l i g h t l y depending on the size of the organism, only worms weighing between 50 and I00 mg (dry weight at I05°C) were used. Twenty worms were placed in i n d i v i d u a l 50 mt beakers containing the e q u i l i brated metal-phase-sand mixture; the beakers were immersed w i t h i n a 20 L, 12°C, aerated aquarium.

The number of worms was l i m i t e d due to d i f f i c u l t i e s

ing large numbers in the size range desired. and feed in the sediment ad l i b i t u m .

in obtain-

The worms were allowed to burrow

An a d d i t i o n a l I0 worms u t i l i z e d as controls

were placed w i t h i n the aquarium in beakers containing only acid-washed sand. Weight losses were determined as less than 10% over the I0 day period.

In the

experiments monitoring uptake from water, 20 worms were placed in the spiked seawater in beakers containing only the acid-washed sand.

The r e s e r v o i r of metal

in the medium phase was large enough that i t acted as in i n f i n i t e r e s e r v o i r in a l l experiments ( i . e . ,

Cs and Cw remained constant with respect to time).

Three worms were removed at each sampling period and placed in a clean aquarium containing only seawater f o r a 24 hr period to purge t h e i r gut contents before analysis. gut.

Dissection showed that t h i s procedure eliminated a l l sediment from the

Flegal and Martin [34] noted that ingested sediment p a r t i c l e s can contribute

s i g n i f i c a n t l y to the measured body burden of trace metals i f precautionary measures are not taken. Analysis A f t e r purging, s a c r i f i c e d worms were dried at IO0°C f o r 24 hr.

Each sample

then was digested twice with I0 m~ of r e d i s t i l l e d concentrated HNO3 by slowly heating on a hot plate to dryness.

A f te r the second digestion the sample was

brought to volume with 1N HNO3 and analyzed by flame atomic absorption spectro-

112

photometry,

Sediment samples were digested and analyzed by the same method ( I 0 m~

of concentrated HNO3 were used f o r each l g of sediment sample). Depuration Experiments To independently estimate values of ke, worms that had been exposed to a solute concentration of metal were placed in a clean sand and sampled f o r a period of 12 days.

Rate constants were calculated from a p l o t of Eq. 8.

RESULTS AND DISCUSSION Depuration The depuration of the organisms a f t e r being subjected to approximately 50 ug/L of Cd in seawater with a sand benthos is shown in Fig. 3.

A two-compartment

depuration is apparent and is modelled as [32]: C = Co(i)e k e ( i ) t

f o r Ci~C
(II)

The c o e f f i c i e n t s from the l i n e s shown ( f i t C = 31e-O'3t

I00

I

(12)

f o r 16~g/g ~C~31 ug/g

and C = 16e-O'O05t I

(13)

f o r C~16ug/g I

'

I

I

I

I

90 80 70 60 50

40 ¸ o_

8 30'

"o L)

20

I

2

Fig. 3.

,

i

4

I

6 Time,

,

I

8 d0ys

by eye) are:

I

I0

,

12

Cd depuration in seawater.

113

I t is assumed for t h i s analysis that the depuration of Cd is independent of the mode of uptake.

Given long times for redistribution between the organism's

tissues, this assumption appears adequate; however, no data were available to substantiate this assumption. Renfro and Benayoun [35] found nearly equal depuration rates for zinc in Nereis diversicolor regardless of uptake from seawater, d e t r i t u s , or f e r r i c hydroxide. Accumulation The results of the accumulation studies are shown in Figs. 4-7.

In each f i g -

ure the data points represent the mean value for three organisms and the vertical bars one standard deviation; in cases where the bars are missing the standard deviation is smaller than the size of the symbol. In a l l experiments with only sand and seawater without cadmium added, the worms did not accumulate cadmium. These control worms were exposed to solution concentrations typical of the natural environment from which they were harvested and hence their tissue concentrations would not be expected to change s i g n i f i cantly. In a l l cases the data could not be adequately f i t techniques because a steady-state was not approached.

by nonlinear regression To obtain accurate para-

meter estimations with nonlinear regression computer programs i t is necessary to use accurate i n i t i a l guesses of ks and ke or the program w i l l either not converge, or w i l l converge to a false minimum [28].

Although values of ke can be estimated

independently from depuration studies, accurate i n i t i a l guesses of ks or kw and convergence can only be made i f the experimental data have approached a steadystate at the end of the experiment. I

I

I

I

I

I

I

I

,4

i2

E Lo

/ / ~

(CdlT=50~gI'

.~ 8

_

6 Sond

T / z ~

(CdlT''~g1' yT

][ Y~

i

01

0

Fig. 4.

I

I

I

I

2

3

I 4

I

I

5

6

Time, doys

Uptake of Cd from seawater.

I 7

I 8

114 60

E 50 E

.9

40

O E ~

30

I

O "~ O

20

_ ~ I

Benl)nite

and Sond

I0 / J.

;ond 2

Fig. 5.

ZS

4 6 Time, doys

8

IO

Uptake of Cd from bentonite. I

i

I

'

I

'

I

I

14 E 12 (:3_

,o

o ~"

8

I

I

~

~6

~ d r o x i d [ end Send

o ,3,,

I

Fig. 6.

I

2

I

I

I

i

4 6 Time, deys

i

I

8

Uptake of Cd from f e r r i c hydroxide.

I0 E

8 6

Humic

cJ

I

2

0

Fig. 7.

~ 2

Send

--

4 6 Time, doys

8

Uptake of Cd from humic acid.

I0

115

Although bioaccumulation studies f o r long periods (28-150 days) to reach steady-state conditions have been reported [27,31], there are several drawbacks in long term studies which l i m i t t h e i r use. f o r the v a r i a b i l i t y

F i r s t , there is a general tendency

about the mean to increase with time; t h i s v a r i a b i l i t y

inherent property of a population of animals. flow-through systems in which i t sediments and water.

is d i f f i c u l t

is an

Second, long term studies require to maintain e q u i l i b r i u m between

T h i r d , the longer an organism is kept under laboratory con-

d i t i o n s , the greater the l i k e l i h o o d that physiological changes w i l l occur that will

influence the rate constants.

The accumulation rates can be estimated by assuming depuration to be n e g l i g i b l e at small t.

For t h i s period the accumulation is zero-order with respect to the

concentration in the organism; a l i n e a r regression analysis can be used to e s t i mate values of k* or k*. The length of time f o r which t h i s s i m p l i f i c a t i o n is s w adequate can be determined by expansion of the exponential terms in Eq. 9 i n t o a Taylor Series as:

J k* ~ ks(J) Cs(J) C = [ w Cw+ - C (i)][ke(i)t ke(i)__ o

(ke(i)t) 2 - - - + 2

(ke(i)t) 3 - - + 6

""

.] + C ( i ) o " (14)

Thus, i f the q u a n t i t y : k e ( i ) t j 0.3, the higher order terms become n e g l i g i b l e as compared to k e ( i ) t ,

and Eq. 14 can

then be approximated as:

J C = (k~ Cw + Z k~(i) Cs(J) - C o ( i ) k e ( i ) ) t + Co(i)

(15)

Based on the value of k e ( i ) f o r Cd over a body burden of less than 16 ug/g, Eq. 15 should apply f o r t < 60 d.

For C > 16 ~g/g, however, l i n e a r i t y can only

be applied f o r t < 2.3d. Eq. 15 was used to c a l c u l a t e k* and k* values f o r uptake from bentonite w s Fe(OH) 3, humic acid, and seawater from Figs. 4-7 (see Table 2). C l e a r l y , the best f i t

of data were obtained f o r seawater and the poorest f i t

associated with

the humic acids. Although the estimated value of k* was several orders of magnitude higher than w the values of the kS's, the product of k*w wC was only s l i g h t l y greater than k*s Cs f o r Fe(OH)3 and humic acid and lower than k*s Cs f o r bentonite.

Because the solu-

t i o n concentration of Cd (50 ~g/L) was much higher than those t y p i c a l l y encountered in the marine environment, these r e s u l t s suggest that sediment phases could be the more s i g n i f i c a n t mode of Cd uptake f o r Abarenicola p a c i f i c a .

116 TABLE 2 Calculated values of the uptake rate constant f o r Cd Geochemical Phase

k~(J)Cs(J)

k~(j) Cs(J) ug/g

ug/g-days 1.4 a 5.2 0.7 0.33

Seawater Bentonite Fe(OH) 3 Humic Acid

0.05 b 3.8 3.4 0.8

da~s-I 28c 1.4 0.19 0.41

a k*w Cw bC W

c

k*

W

The r e l a t i v e uptake from various phases and seawater f o r two t y p i c a l marine sediments are plotted in Fig. 8.

The phases are assumed in e q u i l i b r i u m with

seawater as shown in the isotherms in Fig. I .

These r e s u l t s show that uptake of

sediment-bound Cd, e s p e c i a l l y the clays, is more important than uptake from water As such, these organisms may represent a s i g n i f i c a n t source of cadmium to higher t r o p h i c levels in marine foodchains.

100

Humlcs -Woler ~Fe(OH)3

Noset -Humics "Fe(ON)5

"Cloy

"Cloy

8C

60

=~ 4o 2C

0 5 % Fe(OH) I.:5% HA 5 0 % Cloy 4 8 % Sond

Fig. 8.

0 5 % Fe(OH)~ 5% HA 5 0 % Cloy 4 8 % $ond

Relative uptake of Cd for two typical marine sediments.

CONCLUSIONS A kinetic model was developed which was used to estimate the relative accumulation of cadmium from sediment phases and seawater under laboratory conditions. This model shows that bentonite clay and Fe(OH)3 are larger sources of Cd than seawater for the deposit-feeding polychaete worm, Abarenicola pacifica, under the conditions of this study.

117 ACKNOWLEDGMENT This research was supported by funds provided by the U.S. Department of the I n t e r i o r , Office of Water Research and Technology. REFERENCES 1 G. W. Bryan, Heavy metal contamination in the sea, in R. Johnson, (Ed.), Marine P o l l u t i o n , Academic Press, London, 1976, Ch. 3, pp. 185-302. 2 H. Bowen, Trace Elements in Biochemistry, Academic Press, London, 1966, 291 pp. 3 G. G. Polikarpov, Radioecology of Aquatic Organisms, Reinhold, New York, 1966, 314 pp. 4 E. D. Goldberg, The biogeochemistry of trace metals, in J. W. Hedgpeth, (Ed.), Treatise on Marine Ecology and Paleoecology, I , Memoir 67, Geological Society of America, (1957) pp. 345-358. 5 R. R. Brooks and M. G. Rumsby, The biogeochemistry of trace element uptake by some New Zealand bivalves, Limnol. Oceanogr., I0 (1965) pp. 521-527. 6 B. H. P r i n g l e , D. E. Hissong, E. L. Katz, and S. T. Hulawka, Trace element accumulation by estuarine mollusks, J. of the Sanitary Engineering D i v . , American Society of C i v i l Engineers, 94 (1968) pp. 455-475. 7 D. S. McLusky, Osmoregulation in Corophium v o l u t a r - The e f f e c t of s t a r v a t i o n , Comp. Biochem. P h y s i o l . , 35 (1970) pp. 303-306. 8 D. A. Wolfe and T. R. Rice, Cycling of elements in e s t u a r i e s , Fishery B u l l e t i n , 70 (1972) pp. 959-972. 65Zn 9 W. D. Renfro, Transfer of from sediments by marine polychaete worms, Mar. B i o l . , 21 (1973) pp. 305-316. I0 T. Ueda, R. Nakamura, and Y. Suzuki, Comparison of ll5mcd accumulation from sediments and seawater by polychaete worms, B u l l . Japanese Soc. Sci. Fishe r i e s , 42 (1976) pp. 299-306. I I S. N. Luoma and E. A. Jenne, Factors a f f e c t i n g the a v a i l a b i l i t y of sedimentbound cadmium to the deposit-feeding clam, Hacoma b a l t h i c a , in C. E. Cushing, (ED.), Radioecology and Energy Resources, Ecological Society of America Special Publ. No. I , (1976), pp. 283-290. 12 S. N. Luoma and E. A. Jenne, The a v a i l a b i l i t y of sediment-bound cobalt, s i l v e r , and zinc to a deposit-feeding clam, in R. E. Wildung and H. Drucker, (Ed.), B i o l o g i c a l Implications of Metals in the Environment, 213, NTIS, S p r i n g f i e l d , VA, 1977, pp. 213-230. 13 J. W. Neff, R. S. Foster, and J. F. Slowey, A v a i l a b i l i t y of sediment-adsorbe~ heavy metals to benthos with p a r t i c u l a r emphasis on deposit-feeding infauna, Technical Report D-78-42, U.S. Army Engineer Waterways Experiment S t a t i o n , Vicksburg, MS, 1978, 286 pp. 14 S. Ray, D. McLeese, and D. Pezzack, Accumulation of cadmium by Nereis v i r e n s , Arch. Environ. Contam. T o x i c o l . , 9 (1980) p. I . 15 S. M. Oakley, P. O. Nelson, and K. J. Williamson, Model of trace-metal part i t i o n i n g in marine sediments, Environ. Sci. Technol., 15 (1981) pp. 474-480. 16 R. J. Davies-Colley, Estuarine sediment controls in trace metal d i s t r i b u t i o n s , Ph.D. Thesis, Oregon State U n i v e r s i t y , 1981, 224 pp. 17 E. A. Healy and G. P. Wells, Three new lugworms (Arenicolidae, Polychaeta) from the North P a c i f i c area, Proc. Zool. Soc. London, 133 (1959) pp. 315-335. 18 L. D. Oglesby, Salt and water balance in lugworms (Polychaete: A r e n i c o l i d a e ) , w i t h p a r t i c u l a r reference to Abarenicola p a c i f i c a in Coos Bay, OR, B i o l . B u l l . , 145 (1973) pp. 180-199. 19 J. Hylleberg, Selective feeding by Abarenicola p a c i f i c a with notes on Abarenicola vagabunda and a concept of gardining in lugworms, Ophelia, 14 (1975) pp. 113-137. 20 K. D. Hobson, The feeding and ecology of two North P a c i f i c Abarenicola species (Arenicolidae, Polychaeta), B i o l . B u l l . , 133 (1967) pp. 343-354. 21 K. Fauchald and P. A. Jumars, The d i e t of worms: A study of Polychaete feeding g u i l d s , Oceanogr. Mar. B i o l . Ann. Rev., 17 (1979) p. 193.

118

22 K. R. Tenore, R. B. Hanson, B. E. Dornseif, and C. i~. Wiederhold, The e f f e c t of organic nitrogen supplement on the u t i l i z a t i o n of d i f f e r e n t sources of d e t r i t u s , Limnol. Oceanogr., 24 (1979) pp. 350-355. 23 K. R. Tenore, Growth of C a p i t e l l a capitata cultured on various levels of d e t r i t u s derived from d i f f e r e n t sources, Limnol. Oceanogr., 22 (1977) pp. 936941. 24 K. R. Tenore and U. K. Gopalan, Feeding e f f i c i e n c i e s of the polychaete Nereis virens cultured on hard-clam tissues and oyster d e t r i t u s , J. Fish. Res. Board Can., 31 (1974) pp. 1675-1678. 25 D. G. Kay and A. E. B r a f i e l d , The energy r e l a t i o n s of the polychaete Neanthes (=Nereis) virens (SARS), J. of Animal E c o l . , 42 (1973) pp. 673-692. 26 G. E. Blau, W. B. Neely, and D. R. Branson, Ecokinetics: A study of the fate and d i s t r i b u t i o n of chemicals in laboratory ecosystems, J. Amer. I n s t . Chem. Engr., 27 (1975) pp. 854-861. 27 J. L. Hamelink, Current bioconcentration test nlethods and theory, in F. L. Mayer and J. L. Hamelink, (Eds.), Aquatic Toxicology and Hazard Evaluation, Amer. Soc. f o r Testing and M a t e r i a l s , 1977, pp. 149-161. 28 P. J. Gehring, P. G. Watanabe, and G. E. Blau, Pharmokinetic studies in evaluation of the t o x i c o l o g i c a l and environmental hazard of chemicals, in M. A. Mehlman, et al (Eds), Advances in Modern Toxicology, VoI. I , Wiley, New York (I~76), pp. 195-270. 29 R. A. Goldstein and J. W. Elwood, A two-compartment, three-parameter model f o r the absorption and r e t e n t i o n of ingested elements by animals, Ecology, 52 (1971) pp. 935-939. 30 J. W. Elwood and L. D. Eyman, Test of a model f o r p r e d i c t i n g the body burden of trace contaminants in aquatic consumers, J. Fish. Res. Board Can., 33 (1976) pp. 1162-1166. 31 F. L. Harrison, Effect of physiochemical forms of trace metals on t h e i r accumu l a t i o n by bivalve mollusks, in E. A. Jenne, (Ed.), Chem. Modeling in Aqueous Systems, ACS Symposium Series No. 93, Washington, D.C., 1979, Ch. 27, pp. 611633. 32 V. A. F i l o v , A. A. Golubev, E. I. L i n b l i n a , and [~. A. Tolokontsev, Q u a n t i t a t i v e Toxicology, Wiley, i~ew York, 1979, pp. 144-147. 33 T. Lindstrom, Oregon State Univ. Dept. of S t a t i s t i c s , personal communication. (1980) 34 A. R. Flegal and J. H. Martin, Contamination of b i o l o g i c a l samples by ingested sediment, Mar. P o l l . B u l l . , 8 (1977) pp. 90-92. 35 W.C. Renfro and G. Benayoun, Sediment-worm i n t e r a c t i o n s : t r a n s f e r of 65Zn from marine s i l t by the polychaete Nereis d i v e r s i c o l o r , in C. E. Cushing, (Ed.), Radioecology and Energy Resources, Ecological Society of America, 1976, pp. 250-255.