The English- Wabigoon River System: IV. Interaction between Mercury and Selenium Accumulated from Waterborne and Dietary Sources by Northern Pike (Esox Iucius)

MICHAEL A. TURNER AND ALISON L. SWICK

Freshwater HnsEiEuEe, Department of Fisheries and Oceans, 501 University Crescent, Winnipeg, Man. R3T 2N6

TURNER, M. A., AND A. E. SWICK. 1983. The English-Wabigoon River system: IV. Interaction between mercury and selenium accumulated from waterborne and dietary sources by northern pike (Esm kercius). Can. 5. Fish. Aquat. Sci. 40: 2241 -2258.

Although selenium is a pollutant released by several industries, it is also an essential nutrient that protects mammals against mercury intoxication. When added to aquatic eco- systems, selenium is bioaccumulated readily and can reduce mercury accumu8ation in some biota. Using a predator-prey experimental model, we investigated both the route of selenium uptake and the mechanism of reduction in mercury accumu8ation. Young northern pike (Esox &MC~US) and yellow perch (Bercaflavescens) were caged in situ in mercury-contaminated Clay Lake, northwestem Ontario. Pike were held in water containing trace 4c0.2 pg Se/L) or elevated (4.5-6.4 kg Se/L) concentrations of selenium and were able to accumulate "%g and '"e from food (yellow perch) only, water only, or from food and water. Control pike accumulated as much as 20 times more '%e from food than from water, assimilating -30% of selenium in food. With increased levels of selenium in water (around 5 pg Se/L), food and water were sf similar importance as sources. Waterborne selenium did not alter either the amount of 2 0 3 ~ g accumulated from water or its subsequent partitioning among the pike tissues sampled. When elevated in food, selenium decreased both the body burden of '03Hg in pike and the proportion in muscle. Ht is inferred that selenium added to aquatic ecosystems, and incorporated subsequently in the food web, would interfere with biomagnification of mercury. Furthermore, future studies of selenium toxicity in fish should emphasize its accumulation from food.

TURNER, M. A. , AND A. L. SWICK. 1983. The English-Wabigoon River system: IV. Interaction between mercury and selenium accumulated from waterborne and dietary sources by northern pike (Esox lucius). Can. J . Fish. Aquat. Sci. 40: 224 1 - 2250.

Bien que le sClCniurn soit un contaminant BibCrC par plusieurs industries, il est en mkme temps un nutriment essentiel protkgeant Bes mammifhres contre I'intoxication par le mercure. AjoutC au systkme aquatique, le stlknium est facilemept bioaccumulk et p u t dirninuer, dans certaines biocknoses, B'accumulaticpn du mercure. A I'aide d'un modhle expkrimesltal prCcfateur-proie, nous avons CtudiC a la fois la voie d'assimilation du sClknium et le rnkca- nisme de &duction de l'accumulation de mercure. Be jeunes brochets (Esox luciers) et prchaudes ~Percaflavescens) ont kt6 placks dans des cages in situ dans Ie lac Clay, dans le nord-ouest de I'Ontario, contarnink par le mercure. Les brochets ont CtC maintenus dans de l'eau contenant du sClCnium a l'Ctat de traces (<0,2 pg Se/L) ou de fortes concen- trations (4,5-6,4 ~g Se/L), et ils ont pu accurnuler 2 0 3 ~ g et '%e de la nourriture seulement (perchaudes), de B'eau seulement, ou de la noumiture et de l'eau. Les brochets tkmoins accumulent jusqu'a 20 fois plus de 35Se de la noumiture que de l'eau, assirnilant -30 96 de stlCnium de la nouniture. Aves des augmentations de sClCnium dans l'eau (environ 5 pg Se/E), la nourriture et l'eaaa sont d'importance Cga%e comme sources. Le sildnium contenu dam l'eau me modifie ni la quantitt de 2 0 % ~ accumulC partir de l'eau, ni sa rkpartition substqulente parmi les eissus des brochets CchantillsnnCs. h r s q u e prCsent en plus fortes concentrations daws la nourriture, %e sklknium diminue k la fois la charge corporelle de 'O%g chez les brochets et la proportion dans Be muscle. On en dCduit que le sClCnium ajoutC aux 6cosystkmes aquatiqtses et incorpork subskquemment dans Ie rkseau alimentaire interfkrerait avec la bioamp%ification du mercure. En outre, on devrait, lors d'ktudes futures sur la toxicite du sCB6nium chez les poissons, souligner son accumulation a partir de la nourriture.

Received September 2, 1982 Accepted August 24, 1983

Resu Be 2 septembre 1982 Accept6 le 24 aoDt 1983

Printed in Canada (57066) Imprim6 au Canada (J7064)

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y E

AST

CA

RO

LIN

A U

NIV

ER

SIT

Y o

n 08

/31/

13Fo

r pe

rson

al u

se o

nly.

2242 CAN. 9. FISH. AQUAT. SCI., VOL. 40, I983

SELENIUM is both an essential nutrient and an industrial pollu- tant (reviewed by DeMayo et al. 1979 and Vokal-Borek 1979). When added to aquatic ecosystems at either trace (<0.2 pg Se/L) or higher 41 - 100 yg Se/L) concentrations, Se can move rapidly from water to sediments (Hesslein et al. 1980; Jackson et al. 1980; Wudd et al. 1980; Turner and Rudd 1983). Aquatic biota accumulate Se efficiently at concen- trations in water ranging from <0.2 to 100 pg Se/L (Rudd et a8. 1980: Turner and Rudd 1983). Although aquatic biota can aecumuilate both inorganic and organic Se compounds directly from water (Sandholm et al. 1973; Hodson et aB. 19801, laboratory aquarium experiments indicate that food is also important (Sandholm et al. 1973). Experiments in large en- closures also suggest that food may be the dominant source of Se for aquatic biota (Rudd et al. 1980). However, experi- mental demonstration of the relative importance of food and water for Se uptake in natural ecosystems is lacking.

Careful addition of Se to watercourses, at low concen- trations, has been suggested as an ameliorative procedure for systems contaminated by point-source discharges of Hg (Rudd et al. 1980; Turner and Rudd 1983). When present in food contaminated by Hg, Se may decrease or prevent Hg poisoning in mammals, in spite sf frequently increasing the retention of Hg (Ganther et a%. 1972; Chang et al. 1977; Friedman et a]. 1998). Hn short-term aquarium experiments, Kim et al. (1977) pretreated northern creek chubs (Senlotilur; a~romcac.ulah8tus) with Se02 added to water (3 mg Se/L). Thereafter, chubs were protected from otherwise toxic con- centrations of inorganic Hg (>70 yg Hg/L), but the rela- tionship between Hg concentrations in water and subsequent accumulation of Hg was erratic. Se concentrations of I0 and BOO l j ~ g Se/L in water, added initially as Na2Se03, reduced Hg accumulation in pear1 dace (Sernothlus margnrita) and crayfish (Orcomectes virilis) in aquatic ecosystem experi- ments (Rudd et a%. 1980; Turner and Wudd 1983). Selenium also reduced accumulation of ")'pHg in white suckers (Catos- tornus comrnsraorzi) and possibly did so at 1 yg Se/L in yellow perch (Bercu jirsvescens) (Turner and Rudd 1983). Although 100 pg Se/L increased the rate of movement of 203 Hg from water to sediments, neither sedimentation nor chemical speciation of ""Hg was much changed at I or I0 pg Se/L (Turner and Rudd 19833, The mechanisms underlying the influence sf Se on Hg bioaccumulation remain unclear.

Our objective was to assess the relative importance of water and food in the bioaccumulation of Hg and Se by predaceous fish at both trace and elevated concentrations of Se in water and to determine whether added Se would decrease the trans- fer of Hg between trophic levels. This project was con- ducted as part of a research program on the Mg-contaminated NTabigoon River system (Wudd et a!. 1980, 1983).

Methods

To assess the influence of elevated Se on accumulation of Hg and Se from both food (yellow perch) and water by north- ern pike (ESOX E~~c~us) , fish were held in cages in a sheltered bay of Clay Lake, northwestern Ontario (50"03'N, 93"3Q1W; Armstrong and Hamilton 1973). These experiments began Aug . 15, 1979. approximately 1 mo after the beginning of the Hg amelioration by Se experiment (Turner and Rudd 1983).

In one experiment, cages were positloned within water-tight polyethylene-walled cylinders (1.7 m deep. 10 rn in diameter, and - 130 m"o1ume) which enclosed lake water and were sealed into the sediments. The enclosures are described further in Turner and Rudd (1983). Five miIliCuries of 2 U % g ( ~ 0 3 ) 2 and 3 mCi of H2'Se03 ( I Ci = 37 GBq; New England Nuclear) were added Initially to a control enclosure. Sufficient carrier was added with the 2 " 3 ~ g to yield a concen- tration of about 15 ng Hg/L after dilution in the enclosures. The final concentration of Se after dilution of the added 75Se and cmie r Se was below the analytical detection limit of 0.2 pg Se/L. A second enclosure also received 2 " 1 ~ g ( ~ 0 3 ) 2 , but the H 2 7 5 % e ~ s was mixed previously with sufficient Na2%e03 to yield an initial concentration of 10 k g Se/L. Methods for collection of water samples, their fractionation, and radioassay are presented in Rudd and Turner (1983).

To quantify aceumu%atisn of Hg and Se from food and water, predators (young northern pike) were exposed to '03Hg and 7 ' ~ e in food (young-of-the-year yellow perch) and water or in water alone (Fig. BA). Hn a comborative experiment, pike were exposed to radioisotopes through consumption of radialabeled perch in the absence of radioisotopes in the sur- rounding water (Fig. BB). Each experiment had two groups: a control, wigk a trace amount sf Se (C0.2 ~g Se/L), and another group ta which Se was added.

Fish for these experiments were obtained by seining along a beach in Clay Lake. Northern pike of -35 g and yellow perch of -2 g were selected and assigned randomly to experi- mental treatments.

In the main experiment, three fish cages were placed in each l 0-m-diameter enclosure (Fig. 1 A). Cages (1.2 X 1.2 X

1.2 m) were constructed wigk wooden frames and untreated Ace-style nylon netting with 0.64-cm mesh (Nichols Net and Twine Co.). In each of the control and added Se conditions, there were two groups of pike. All pike in this experiment were exposed to waterborne 75%e and 20'Hg, but one group of pike could also consume radiolabeled perch enclosed in the same cage. After 1 and 2 wk, three pike were taken from each treatment enclosure and radioassayed for whole body and tissue radioisotope concentrations. In addition, radioisotope concentrations in whole bodies of three perch were deter- mined for each combination of Se (control or added Se) and duration (I-, 2-, or 3-wk exposure). Perch were placed in cages 1 wk prior to addition of the pike and could accumulate radioisotopes from both water and food (e. g . zooplankton) The nominal food ration for each pike was four perch per week. The number of perch remaining in each cage at the end of a sampling period was determined so that the ration could be adjusted accordingly.

In the corroborative experiment, two additional cages were placed outside the 10-m-diameter enclosures, each within a larger cage of wire mesh (Fig. 1B). Bn absence of exposure to radioisotopes in the surrounding water during this experi- ment, pike were fed perch that bad been labeled previously with '03Hg and 75Se, in cages within the control and elevated Se enclosures. The nominal ration was four perch per pike. Selenium levels in perch in the Se-treated group were elevated compared with controls by approximately 0.8 pg Se/g (wet wt). Pike were collected 6 d after addition of the perch and sampled as in the earlier experiment.

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y E

AST

CA

RO

LIN

A U

NIV

ER

SIT

Y o

n 08

/31/

13Fo

r pe

rson

al u

se o

nly.

TURNER AND SWICK: Mg-Se INTERACTIONS IN PREDACEOUS FISH 2243

Fish were frozen using dry ice immediately after sampling. Samples were kept frozen until dissection into several tissues: dorsal skeletal muscle, liver, gill (including arch), skin, gas- trointestinal musculature, and carcass (whole body excluding other tissues). Gastrointestinal contents were extruded from the gut and collected separately but were not included in estimates of either whole body concentrations or radioisotope consumed. The gut was rinsed with tap water and prepared separately for radioassay. Samples were then refrozen until analysis.

Radioisotope concentrations in whole bodies of pike, ex-

Assimilation efficiency

- - (total radioisotope consunaed) - (egestion) (total radioisotope consumed)

- - (residual radioisotope in body sf pike)

(total radioisotope consumed)

- - (mean weight of all pike) x (mean concentration

(mean No. of perch consumed/pike2) x

Calculations were made for each group of three pike and not for individuals, because the amount of radioisotope ingested by each group was known better than that of an individual. The assimilation efficiency reported for week 2 represents a mean for the 2-wk period.

Results

In the control enclosure, concentration of 7%e in the water cdumn was relatively constant at approximately 1 125 cpm/ l during the 3 wk of the experiment (Fig. 28). In the Se en- closure, 7%e moved to the sediments during the experiment (Turner and Wudd 1983) declining from 12'75 to 900 cpm/L in water, with corresponding total Se concentrations of -6.4 and 4.5 pg Se/L.

The chemical partitioning of Se in water was also different between these two enclosures. Hn the control enclosure, -60% of 7?Se was associated with nonpolar dissolved organic substances and about 25 and 15% in ionic or particulate forms. In the Se enclosure, ionic species predominated (-70%), with the remainder associated largely with nonpolar

'Accumulations of radioisotopes from food and water were as- sumed to be independent processes as observed for Hg in rainbow trout (Salrno gairdneri) (Phillips and Buhler 1978). Mercury-203 and 7 5 ~ e observed to accumulate in the "water-only" group were sub- tracted from the "food plus water" group to yield an estimate of the contribution due to food alone.

'when corrected for perch remaining in the cage and material remaining in the gut, calculated rations for individual control pike were 3.3 and 3.9 perch/wk in weeks 1 and 2, respectively. Come- sponding rations for Se-exposed pike were 2 .2 and 3 .3 percch/wk.

'Weekly radioisotope concentrations in perch were calculated as the arithmetic mean of the eoncentratic>ns observed at the beginning and end of that week. No comection was made for radioisotopes remaining in the gastrointestinal system of the perch.

cluding gastrointestinal contents, were determined from con- centrations in observed tissues and carcass samples. Radio- isotope concentrations in whole bodies of pike and perch, and proportions of radioisotopes in tissue of pike, were examined using factorial analysis of variance (Snedecor and Cochran 1967). Otherwise, lognormal means and variances are pre- sented for each group of pike or perch.

"Assimilation efficiency" (Aoyama and Inoue 1973; Phil- lips and Gregory 19'19) was calculated to determine the effi- ciency of net accumulation of each radioisotope from fwd. This accounts for different amounts of ratdioisotope in perch of the Se-treated and control groups:

of radioisotope in whole body of pike obtained from food')

(mean radioisotope burden in perch whole bodies3)

dissolved organics. Selenium-'75 in perch increased rapidly throughout the

3-wk period in both control and treatment conditions, although there was a suggestion of a lag in uptake during the 1st wk of exposure, especially noticeable in the Se-treated enclosure (Fig. 2B). Differences in specific activity ('"e: Se) between the control and Se enclosures prevent direct com- parison of perch 75Se concentrations.

In the control condition. 7 5 ~ e concentrations in pike al- lowed to feed on 7%e-labeled food were 7 (week I ) and 20 times (week 2) greater (P < 0.001) than when 7?Se was supplied only in water (Fig. 3A, control). With increased concentrations of Se in water, the relative importance of water as a source of 75Se increased (Fig. 3A, Se). Although the concentrations of 75Se in the perch were reduced (Fig. 2B), assimilation of Se from foodstuffs was reduced in the presence of increased concentrations in water (Fig. 3B, Se: food + water vs food). In the control, assimilation of Se from food (perch) was approximately 3Q%, whereas assim- ilation ranged from 8 to 19% with the addition of Se (Fig. 3B, food + water: control vs Se). When Se was increased in food but not supplied in water, as in the corroborative experiment (Fig. IB). assimilation was not very different from that in the control (Fig. 3B, food only).

Partitioning of Se among the tissues sampled, as indicated by tissue to whole body concentrations (Table 1), was not altered greatly by either the amount of Se present (control vs Se) or the route of Se uptake (water vs food and water). In all treatments, the proportion of 7 5 ~ e was highest in the liver (5.8 - 15.0) and lowest in the skeletal musculature (0.21 -0.41). The proportion of 75Se in the gut musculature was somewhat higher in pike fed 75~e-labeled food than in pike with access to "Se in water only ( P < 0.01). This in- crease was reduced in the presence of elevated Se concen- trations in water (Table I ) , which is consistent with the obser- vation of reduced assimilation (Fig. 3B, food + water: control vs Se).

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y E

AST

CA

RO

LIN

A U

NIV

ER

SIT

Y o

n 08

/31/

13Fo

r pe

rson

al u

se o

nly.

CAN. I. RSH. AQUAT. SCI.. VOL. 40, 1983

A. MAbN EXPERIMENT 203 Hg ond "St3 available to p ik in wow and food or in water only

CONTROL ENCLOSURE SEbEN lUM ENCUSURE

E3 CORROBORATORY EXPERIMENT 203 Hg and '%e available to pike in food only

Cage B

PERCH

BAKE WATER SEbENl BBM ENCLOSURE LAKE WATER

4

0 Fi (food orsly)

Cage 2

PIKE (food +water)

04 enclosure

PERCH

B I FIG. 1. Schematics of experimental designs. In the main experiment (A), pike can accumulate '03Hg and 75 Se from food and water, or from water only. in the presence or absence of added Se. In the comobrative experiment (B), radioisotopes are accumulated only by consumption of prey (perch). Arrows represent main mutes of radioisotope naovement. It is probable that perch aceurnulated rdioisvtopes from unknown food sources as well as from water directly.

Concentrations of 203Hg in water were similar in both con- trol and Se enclosures, decreasing to one-half during the ex- periment (Fig. 4A). There were no substantial differences in partitioning of 2 0 3 ~ g among the different chemical fractions: particulate (>0.45 pn), nonpolar dissolved organics, ionic, and undefined.

Throughout the main experiment (Fig. IA), "3Hg in whole bodies of perch continued to increase in both the control and added Se enclosures (Fig. 3B). Mercury -203 concentrations in perch exposed to Se were consistently lower than in control

perch (P - 0.02). Where both Hg and Se radioisotopes could be taken up only

from water, 2 0 3 ~ g concentrations in whole bodies and skeletal muscle of pike were not different between the control and Se conditions (Fig. 5A, water only). Where 2 " 3 ~ g could also be accumulated by consumption of perch, concentrations in whole bodies ( B < 0.03) and skeletal muscle ( B - 0.001 ) of pike were always lower in the presence of added Se (Fig. 5A, food t water). Although this is partly due to the lower amounts of 2 0 3 ~ g ingested by Se-exposed pike relative to control pike, increased Se reduced the assimilation of '"%IHg from food from approximately 15% in the control to 5 - 1 1%

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y E

AST

CA

RO

LIN

A U

NIV

ER

SIT

Y o

n 08

/31/

13Fo

r pe

rson

al u

se o

nly.

TURNER AND SWICK: Hg-Se HNTEKACTIOWS IN PREDACEOUS FISH 2245

A. " ~ e in water Days After Isstope Additbn

Days After Perch Addition

8. Accumulation of7%e in Whole I Bodies of Perch

Days of Exposure

(Fig. 5B, food 4- water). In the food-only experiment (Fig. 18, radioisotsges and added Se present only in food), a reduction in assimilation efficiency of '03Hg of similar magnitude was also observed (8 vs 14%, Fig. 5B, food only), suggesting that Se in food rather than Se in water was responsible.

Where '"%& could be taken up only from the water co1- umn, waterborne Se did not influence partitioning of "%lg among pike tissues (Table 2), not even in gill tissue. In csn- trast, where "'Mg could also be accumulated from food, the proportion of "%g in both the gut (P < 0.001) and skeletal musculature (P - 0.881) was higher than where '03~g could be taken up only from water. These increases of 203Hg in gut and skeletal musculatures observed in the control condition were reduced with exposure to added Se ( P < 0.01 and P < 0.05, respectively) in food and water.

For several reasons we used radioisotopes and did not mea- sure changes in concentration of the stable elements. The initial variability of stable Se and Hg concentrations in the perch and pike would have hindered detection of treatment effects. With addition of the radioisotopes ''%IHg and 75Se, a definite time zero existed beyond which new accumulations of radioisotopes could be compared between test and control conditions. Using the analytical sensitivity of radioisotope techniques, we were also able to avoid the confusing effects of a large chemical addition of Hg. Given the relatively long biological half-life of Hg in fish (reviewed by Huckabee et ale 1979) it is unlikely, however, that added 2 U % ~ would have equilibrated during the experiment with Hg previously in Be fish. The biological half-life of Se is less well known. although it has been determined to be approximately 1 mo in Seikmo gaird~teri (Gissel Nielsen and Gissel-Nielsen 6978). Therefore, it is also unlikely that added 7%e would have equilibrated with Se previously in the pike and perch. Only in the elevated Se condition was 7 5 ~ e used as a radiotracer. Otherwise, we used a comparative approach and not a radio- tracer strategy. By ensuring that both the radioisotope addi- tions and the initial amounts of stable elements in the control and experimental compartments were identical, we could compare accumuBations of each radioisotope between control and test conditions.

Selenium is accurnuIated from both food and water (Fig. 3A and 3B). At Bow concentrations of Se in water (c0.2 ~g

Fm. 2. (A) Selenium-75 concentration in the water colunans of the control and Se enclosures during the periods when fish were exposed to 9 s ~ e . Concentrations shown for the last point are predictions from models fit to earlier data (explained in Turner and Wudd 1983). (B) Seleniham-75 concentrations in whole bodies of perch held in the control (C) and Se (S) enclosures. Each point represents the antilog of the lognormal mean of three individuals. Along the radioisotope axis (left-hand axis), uppel and lower values refer to perch in the control and Se conditions, respectively. Given the known specific activity of 75Se:Se in the Se enclosure, computed amounts sf Se accumulated are also shown (right-hand axis).

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y E

AST

CA

RO

LIN

A U

NIV

ER

SIT

Y o

n 08

/31/

13Fo

r pe

rson

al u

se o

nly.

2246 CAN. J . FISH. AQUAT. SCI., VOL. 40. 1983

A. kumulation of m ~ e in Whole Bodies of Pike

Weeks of Exposure

Weeks of Expowre

FIG. 3. (A) Whole body "Se in northern pike held for I or 2 wk in the control or Se enc8osures. Pike were able to accumulate "Se from food (perch) and water, or from water only. Two standard error bars are shown about each mean of three individuals. The right-hand axis is as described in Fig. 2B. (B) Efficiency of assimilation of 75Se from food (perch) by pike after 1 and 2 wk. To obtain the estimate of the body burden of "Se due to food alone, the uptake of 75Se from water, as measured in the water-only condition (Fig. 3A), was subtracted from the body burdens observed in the food and water condition. In the comoborative, food-only experiment. the contribution of radis- isotopes in f c ~ d to the body burden was observed directly.

Sell,), food web transfers predominate for fish (Fig. 3A; Wudd et al. 1980; Sandholm et al. 1973), although concen- trations in other organisms, such as in zmplankton, depend on water concentrations (Turner and Wudd 1983). At in- creased Se concentrations in water (Fig. EA, 4.5-6.4 pg Se/L), pike accumulated only somewhat less "Se than in the control condition (Fig. 3A, water only: control vs Se), despite the fact that the ambient concentration of radioiso- tope was lower (Fig. 2A). The greater than 25-fold increase in Se concentration in water (e0.2 vs -5 pg Se/L) indicates

that substantially more Se was accumulated from water by Se-exposed pike.

Fish seem able to regulate the amount of Se bioaccum~tlakd to some extent (Hilton et al. 1980; Hodson et al. 8980). Although assimilation of Se appears to be independent sf food Se concentration (Fig. 3B, food only), increased concen- trations of Se in water can reduce assimilation of Se (Fig. 3B, food + water: control vs Se).

Selenium concentrations vary among tissues (Table I ; Hodson et al. 1980; Turner and Rktdd 1983) and partitioning can vary with time as shown in Table 1. Highest concen- trations are observed in the liver (Table 1) and kidney (Hilton et al. 1980; Hodson et al. 1980), both of which have been postulated to be involved with Se regulation and excretion (Hilton et al. 1880).

INTERACTION BEg\.VEEN SELENIUM AND MERCURY

Caged yellow perch, which accumulated radioisotopes from both water and food (e. g. zooplankton), consistent1 y accumulated less 2U%IHg when exposed to added Se ( P - 0.02, Fig. 4B). This was also seen in pearl dace, white suckers, and uncaged perch living in the 10-m-diameter enclosure with an initial water concentration sf 10 pg Se/k (Turner and Wudd 1983). When Se was increased only in the water column (4.5 -6.4 pg Se/L, Fig. 2A), there was no change in either the amount of 2 0 % ~ that pike accumulated from water (Fig. 5A, water only) or the distribution of 2Q%g among tissues examined (Table 2). Because the proportion of methyl to total Hg in water was probably small, -5% (Parks et al. 1980), this effect may also be seen as a lack of action of Se an uptake of inorganic Hg from water.

Control pike, able to accumulate 203Mg from both water and food, obtained from 33% (week 1) to 43% (week 2) of their 2"4Hg body burden from food (Fig. 5A, control: water only vs food + water). Hn both weeks, an assimilation efficiency of - 15% was observed in the transfer of 204Hg from perch (food) to pike (Fig. 5B, coa7itroDoB). This is similar to the observation by Phillips and Gregory (1979) in which pike assimilated 19% of naturally occuHkng methyl mercury in young-of-the-year carp (Cyprin~~s carpio). In contrast, when Se concentrations were increased in perch by 0.05-0.4 yg Se/g (Fig. 2B), assimilation of 'O%g from food declined to between 5 and I I % (Fig. 5B, fwd and water: Se). This was corroborated by the food-only experiment (Fig. 5B, food only: Se) in which Se in perch was elevated by about 0.8 pg Se/g (wet wB) and assimilation efficiency was 8 vs 14% in the controls. These short-term observations imply that the reduction in bioaccu- mulation of 2 a 3 ~ g by fish, observed in in situ ecosystem experiments (Rudd et al. 1980; Turner and Rudd 19831, is due to interference of Se with Hg mobilized through food webs, rather than on Hg accumulated directly from water. gBbsewations of longer duration are required to determine whether the increase from week B to week 2 in percentage assimilation of 203Hg from food in Se-exposed pike (Fig. 5B, food and water: Se) represents a trend. Because a Se-induced concentration-dependent reduction in Hg accumulation in several fish species was observed after 2 mo (Turner and Rudd 1983), we think this is unlikely.

Control pike had proportionately more ?-Ip~g in the gut and

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y E

AST

CA

RO

LIN

A U

NIV

ER

SIT

Y o

n 08

/31/

13Fo

r pe

rson

al u

se o

nly.

TURNER AND SWICK: Hg-Se INTERACTIONS IN PREDACEOUS FISH

TABLE 1 . Ratios of tissue to whole body concentrations of "Se (mean 5 sD, N = 3).

Week I Week 2 Experimental

Tissue condition Water Food + water Water F w d + water

Gill Control

Se

Skin Control

Se

Gut Control

Se

Liver Control

Se

Muscle Control

Se

5.98 (2 1.56)

5.66 (22.49)

1.85 (20.60)

Not measured

H .77 (20.92)

2.29 ( k 1.03)

7.80 (k3.24)

10.84 (k3.24)

0.21 (20. 15)

0.41 (20.35)

skeletal musculatures when accumulating " 3 ~ g from food and water together than from water only (Table 2). This is consistent with the observation that Hg burdens obtained via food and water are additive (Phillips and Buhler 1978). Par- titioning the 203Hg in muscle according ts source indicates that 75-8196 of the muscle a03Wg burden in food- and water- exposed pike was obtained from food in weeks 1 and 2. With increased concentrations of Se in both food and water, there was a larger proportion of 2"3H~ found in the liver in week I ( P - 0.81), with comparatively less in the skeletal (P < 0.05) and gut musculatures (B < 0.01 ; Table 2, food + water: control vs Se, week 2). In contrast with control pike, in weeks 1 and 2, only 44 and 52% of 2 0 3 ~ ~ in muscle of Se-exposed pike was acquired from food. Furthermore, liver 203Mg probably was inorganic (Burrows and Krenkel 8973), so that the comparison between 2 0 3 ~ g burdens of control and Se-exposed pike (Fig. 5A) could underestimate the influence of Se on body burdens of methyl mercury. The liver was also a site for high Se concentrations (Table I). This concurs with the suggestion that the liver is a storage organ for Se in Sakmo gairdneri (Hilton et al. B 980).

Losses sf '03~g from pike were not measured so that it is unknown whether the Se-induced reduction in assimilation of 203 Hg (Fig. 5B, control vs Se) is due to lowered absorption of 2"%g from the gut or to its enhanced depuration. However, the proportion of 2"3Hg in gut musculature of Se-fed pike was reduced relative to controls (P < 0.01, Table 2, food and water). Because the source of exposure, food or water, ap- pars unimportant to the tissue distribution of methyl mer- cury, except perhaps for the tissue involved in its uptake (McKim et al. 1976), it is unlikely that reduced absorption from gut can be the only mechanism involved.

IMPLICATIONS FOR MERCURY AMELIORATION

Selenium supplementation has been suggested as a stm- tagem to reduce the severity of pint-source Hg csntamina- tion, and it may also decrease the bioavailability and toxicity of atmospherically transported Hg (Rudd et al. 1980, 1983; Turner and Rudd 1983). The results of our experiments s u p port these ideas.

Selenium can reduce bioaccumulation of Hg in several nonpredaceous fishes (Fig. 4B; Rudd et al. 1980; Turner and Rudd 1983). It seems probable that this effect would be in- creased further in organisms at higher positions within food webs; i.e. Se may interfere with the biomagnification of Hg. For example, lowered '03Hg concentrations observed in perch (Fig. 4B, B - 0.02) appear to be further reduced in pike by the lowered assimilation of 2"3Hg when accumulated from food sources (Fig. 5B, Se vs control). Additionally, the Se- induced reduction in the proportion of 2Q3Hg in skeletal mus- cle of pike (5 1 LTo of control after 2 wk, Fig. 5A, food and water) may be an amplification of a similar decrease observed in pearl dace (75% of control) exposed for an equal length of time to Se at a concentration of 10 pg Se/L (unpublished data). This suggestion of interference with the transfer of Hg, depending on food web position, is further supported by ob- servation of decreased accumulation of 2" '~g in predaceous aquatic insect larvae (Stakis and C h a o b ~ r u ~ ) living in eco- systems containing added Se (initially at 10 and I00 kg Se/L), without such decreases apparent in the detrivorous insects Hexagereia and Chironsmus (B. E. Townsend, Fresh- water Institute, Winnipeg, Man., personal communication). Therefore, the reduction observed in accumulation of 2 " 3 ~ g in young suckers and perch, but not dace, after 2 mo at 1 pg

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y E

AST

CA

RO

LIN

A U

NIV

ER

SIT

Y o

n 08

/31/

13Fo

r pe

rson

al u

se o

nly.

CAN. J . FISH. AQUAT. SCI., VOL. 40, 1983

A ? ' ~ H ~ in water Days After Isotope Addition

Days After Perch Addition

B. Accumulation of 203~9 in Perch

A. Accumulation of 203~9 in Pike 307 W"er.owly Food + Water

Week I Week 2 g c S , l C % , Week I Week 2

B Assimilation of =HCJ from Food by Pike

FIG. 5 . (A) Concentrat i~~n~ of *'%g in northern pike held for 1 or 2 wk in the control (@) or added Se (S) enclosures. Pike were able to accumulate 'O%g from food (perch) and water, or by uptake from water only. Concentration in skeletal muscle is shown in the hatched areas, while whole bodies are represented by the total height of each bar. Two standard error bars we shown about each mean s f three individuals, (B) Efficiency of assimilation of 203Hg from food (perch) by pike after 1 and 2 wk. To obtain the estimate of the burden of *03EIg due to food alone, the uptake of '0314g from water, as measured in the water-only condition (Fig. 5A), was subtracted from body bur- dens observed in the food and water condition. In the corroborative, food-only experiment, the contribution of radioisotopes in food to the b d y burdens was observed directly.

Fo. 4. (A) Concentrations of "Wg in the water column of the s e / ~ (Turner and Rudd 1983) may be in control (C) and Se (S) enclosures during the periods when perch and predaceous pike were exposed to '"H~. Concentrations shown for the last point are derived from model predictions (explained in Turner and Rudd Se in water does not reduce bioaccumu'ation of 1983). (B) Mercury-203 in whole bodies of perch held in either the Hg from (Fig- 5 A ) 9 levels of Hg do not have to be control ( C ) or Se 4s) enclosures. Each point represents the antilog f t ? d ~ ~ " d either in h e contaminated food or in the consuaner of the lognormal mean of three individuals. Concentrations of U'3Hg for $6 to exert its Hg-detoxifying effect (Chaw et al. 19'97; in perch of the Se and control conditions were significantly different Friedmaan et al. 1978). The ability of Se to reduce Hg acear- (P - 0.02). mulation appears to be exerted via food intake (Fig. 5B).

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y E

AST

CA

RO

LIN

A U

NIV

ER

SIT

Y o

n 08

/31/

13Fo

r pe

rson

al u

se o

nly.

TURNER AND SWICK: Hg-Se lNTERACTIONS IN PREDACEOUS FISH

TABLE 2. Ratios of tissue to whole body concentrations of 20%Hg (mean 2 SD, hr = 3.)

Week 1 Week 2 Experimental

Tissue condition Water Food + water Water Food + water

Gill Control

Se

Skin Control

Se

Gut Control

Se

Liver Control

Se

Muscle Control

Se

1.08 (20.50)

Not measured

Furthermoree, Se is transferred efficiently through food webs (Fig. 3B), so that elevated water concentrations would not have to be maintained continuously if periodic pulses could sufficiently load the food web. Any "addition9' strategy should include monitoring levels in the food web to prevent buildup of unexpected, and potentially dangerous, concentra- tions of Se.

Our work suggests that increased emphasis should be placed on the potential toxicity to fish of elevated Se concen- trations in food. Moreover, before Se can be used as an aquatic ameliorating agent with some degree of confidence, we should assess further both what minimum ratio of Set Hg is effective in reducing assimilaeisaa sf Hg and whether there is any time dependency of this effect.

The guidance and encouragement of J. W. M. Rudd and F. A. J . Amstrong are gratefully acknowledged. The analytical assistance of Eva Sgavicek was appreciated. Erin Bums-Flett radioassayed many of the samples. F. A. J. Armstrong, G. Bmnskill, P. Campbell, B. Hecky, J. H. Klaverkamp, S. Lawrence, J. W. Parks, J. W. M. RusfQ, and D. W. Schindler constructively criticized the manuscript. Without benefit of the eccelogical insight of Gordon Clark, a "minnow-man" and trapper, these experiments could not have occurred. The Freshwater Institute and Camadian Federal and Ontario governments funded these experiments through the Canada Water Act.

AOYAMA, I. , AND Y. BNOUE. 1973. Estimation and evaluation of radioactive contamination through a food web in an aquatic ecosystem (1). J. Radiat. Res. 14: 375-381.

A W M S ~ Q N G , F. A. J., AND A. HAMILTON. 1973. Pathways of mercury in a polluted northwestern Ontario lake, p. 131 - 135. In P. C .

Singer [ed.] Trace metals and metal-inorganic interactions in natural waters. Ann Arbor Science Publishers Hnc., Ann Arbor, MI.

BURROWS, W. D., AND P. A. KWENKEL. 1973. Studies on uptake and loss of methylmercury-203 by bluegills (Lepomi~ macrochiru~ Raf.). Environ. Sci. Technol. 7: 1127-1130.

CHANG, L. W., A. W. DUDLEY, M. A. DUDLEY, H. E. GANTHER, AND hq. L. SUNDE. 1977. Modification of the neurotoxic effects of methyl mercury by selenium, p. 275-282. In L. Woizin, H. Shiraki, and N. Grecvic [ed. ] Neurotoxicology . Raven Press, New York. NY.

DEMAYO, A., M. C. TAYLOR, AND S. W. REEDER. 1979. Guidelines for surface water quality. Qol. 1. Inorganic chemical substances. Selenium. Inland Waters Directorate, Department of Environ- ment, Water Quality Branch, Ottawa, Qnt. 21 p.

FRIEDMAN, M. A., L. R. EATON, AND W. H. CARTER. 1978. Pr0tec- tive effects of freeze dried swordfish on methylmercury chloride toxicity in rats. Bull. Enviran. Contam. Toxicol. B 9: 436-443.

GANTHER, H. E., C. GOUDIE, M. L. SUNDE, M. J. KOPECKY, P. WAGNER, S.-H. OH, AND W. 6. HOEKSTBA. 1972. Selenium: relation to decreased toxicity of methylmercury added to diets containing tuna. Science (Washington, DC) 175: 1 122- 1 124.

GISSEL NIBLSEN, M., AND G. GISSEL-NIELSEN. 1978. Sensitivity of trout to chronic and acute exposure to selenium. Agric. Environ. 4: 85-91.

HESSLEIN, R. H., W. S. BROECKER, AND B. W. SCHIMDLER. 1980. Fates of metal radiotracers added to a whole lake: sediment- water interactions. Cam. J . Fish. Aquat. Sci. 37: 378-386.

HILTON. J. W., P. Q. HQDSBN, AND S. B. SLHNGER. 1980. The require- ment and toxicity of selenium in rainbow trout (SaPmo gairdneri). J. Nutr. 110: 2527-2535.

HODSON, P. Q., 14. J . SPRY, AND B. W. BLUNT. 1980. Effects on rainbow trout (J;almo gairdneri) of a chronic exposure to water- borne selenium. Can. J . Fish. Aquat. Sci. 37: 233-240.

HUCKABEE, B. W., B. W. ELWOOD, AND S. 6. HILDEBRAND. 1979. Accumulation of mercury in freshwater biota, p. 277-302. In

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y E

AST

CA

RO

LIN

A U

NIV

ER

SIT

Y o

n 08

/31/

13Fo

r pe

rson

al u

se o

nly.

22563 CAN. S . FISH. AQUAT. SCI., VOL. 40, 1983

J. 0. Nriagu [ed.] The bisgwchemistry of mercury in the envi- ronment. Elsevier/North-Holland Biomedical Press, New York, NY.

JACKSON, T. A., G. KIPPHUT, R . HESSLEIN, AND D. W. SCHINDLER. 1980. ExprimentaE study of trace metal chemistry in soft-water lakes at different pH levels. Can. J. Rsh. Aquat. Sci. 37: 384-402.

KIM, J. H . , E. BIRKS, AND J. F. HEISINSER. 1977. Protective action of selenium against mercury in northern creek chubs. Bull. Envimn. Contam. Toxicol. 17: 132- 136.

MCKIM, J . M. , G. F. OLSON, G. w. HOKOMBE, AND E. P. HUNT. 1976. Long-term effects s f methytmercuric chloride on three generations of brook trout (Sffkvelinusf~nrina/is): toxicity, accu- mulation, distribution, and elimination. J. Fish. Res. Board Can. 33: 2726-2739.

PARKS, J. W., J. D. HOLLINGER, AND P. M. ALMOST. 1980. The transport and dynamics s f mercury in the Wabigoon River and Clay Lake. dn T. A. Jackson [ed.] Mercury pollution in the Wabigoon-English River system of northwestern Ontario, and possible remedial measures. Progress report for Canada Water Act and Government of Ontario. 145 p.

Ppn1L~lP.5, G. R., AND B. R. BUMLBW. 1978. The relative contributions of methytmercury from food or water to rainbow trout (Saltno gairdneri) In a controlled laboratory environment. Trans. Am. Fish. Soc. 107: 853-861.

PHILLIPS, G. R., AND K. W. GREGORY. 1979. Assimilation efficiency

of dietary methylmercury by northern pike (Esox lucdlcs). J. Fish. Res. Board Can. 36: 1516-1519.

RUDD, J . W. M., AND M. A. TURNER. 1983. The English- Wabigoon River system: II. Suppression of mercury and selenium bis- raccumulatisn by suspended and bottom sediments. Can. J . Fish. Aquat. Sci. 40: 221 8-2227.

R u m , J . &9'. M., M. A. TURNER, A. FUWUTANT, B. E. TOWNSEND, AND A. SWICK. 1983. The English-Wabigoon River system: 1. A synthesis of recent research on the English-Wabigson River system with a view towards mercury amelioration. Can. J . Fish. Aquat. Sci. 40: 2206-2217.

Rum, J . W, M., M. A. TURNER, B. E. TOWNSEND, A. %WICK, AND

A. FUWUTANB. 1980. Dynamics of selenium in mercury con- taminated experimental freshwater ecosystems. Can. J. Fish. Aquatat. Sci. 37: 848-857.

~ANDHQLM, M., H. E. B~)KSANEN, AND L. &SONEN. 1973. Upt&e of selenium by aquatic organisms. Eimnol. Oceanogr. 19: 496 - 499.

S N E D E ~ W , G . W., AND W. G. COCHRAN. 1967. Statistical methods. 6th d. The Iowa State University Press, Ames, IA.

TURNER, M. A., AND 9. W. M. RUDD. 1983. The English-Wabigoon River system: III. Selenium in take enctosures: its geochemistry, bioaccurnuiation, and ability to reduce mercury bioascumula- tion. Can. J. Fish. Aquat. Sci. 40: 2228-2240.

VOKAL-BORBK, H. 1979. Selenium. Univ. Stockhotm Inst. Phys. Rep. 79-16: 206) p.

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y E

AST

CA

RO

LIN

A U

NIV

ER

SIT

Y o

n 08

/31/

13Fo

r pe

rson

al u

se o

nly.

This article has been cited by:

1. D. Sampaio da Silva, M. Lucotte, S. Paquet, G. Brux, M. Lemire. 2013. Inverse mercury andselenium concentration patterns between herbivorous and piscivorous fish in the Tapajos River,Brazilian Amazon. Ecotoxicology and Environmental Safety . [CrossRef]

2. David C. Depew, Niladri Basu, Neil M. Burgess, Linda M. Campbell, Ed W. Devlin, Paul E.Drevnick, Chad R. Hammerschmidt, Cheryl A. Murphy, Mark B. Sandheinrich, James G. Wiener.2012. Toxicity of dietary methylmercury to fish: Derivation of ecologically meaningful thresholdconcentrations. Environmental Toxicology and Chemistry 31:7, 1536-1547. [CrossRef]

3. Michael K. Saiki, Barbara A. Martin, Thomas W. May, William G. Brumbaugh. 2012. Assessmentof Two Nonnative Poeciliid Fishes for Monitoring Selenium Exposure in the Endangered DesertPupfish. Water, Air, & Soil Pollution 223:4, 1671-1683. [CrossRef]

4. Poul Bjerregaard, Susanne Fjordside, Maria G. Hansen, Maya B. Petrova. 2011. Dietary SeleniumReduces Retention of Methyl Mercury in Freshwater Fish. Environmental Science & Technology45:22, 9793-9798. [CrossRef]

5. Patrice Couture, Greg PyleField studies on metal accumulation and effects in fish 31, 417-473.[CrossRef]

6. Dan-Yi Yang, Xu, Ye, Yu-Wei Chen, Nelson Belzile. 2010. Inverse relationships between seleniumand mercury in tissues of young walleye (Stizosedion vitreum) from Canadian boreal lakes. Scienceof The Total Environment 408:7, 1676-1683. [CrossRef]

7. Nelson Belzile, Yu-Wei Chen, Dan-Yi Yang, Hoang-Yen Thi Truong, Qiu-Xiang Zhao. 2009.Selenium Bioaccumulation in Freshwater Organisms and Antagonistic Effect against MercuryAssimilation. Environmental Bioindicators 4:3, 203-221. [CrossRef]

8. Helena do A. Kehrig, Tércia G. Seixas, Elisabete A. Palermo, Aida P. Baêta, Christina W. Castelo-Branco, Olaf Malm, Isabel Moreira. 2009. The relationships between mercury and selenium inplankton and fish from a tropical food web. Environmental Science and Pollution Research 16:1,10-24. [CrossRef]

9. Sean M. Strom. 2008. Total Mercury and Methylmercury Residues in River Otters (Lutracanadensis) from Wisconsin. Archives of Environmental Contamination and Toxicology 54:3,546-554. [CrossRef]

10. Lina Jin, Lina Liang, Guibin Jiang, Ying Xu. 2006. Methylmercury, total mercury and totalselenium in four common freshwater fish species from Ya-Er Lake, China. EnvironmentalGeochemistry and Health 28:5, 401-407. [CrossRef]

11. Gregory G. Pyle, James W. Rajotte, Patrice Couture. 2005. Effects of industrial metals on wild fishpopulations along a metal contamination gradient. Ecotoxicology and Environmental Safety 61:3,287-312. [CrossRef]

12. Steven J. Hamilton. 2004. Review of selenium toxicity in the aquatic food chain. Science of TheTotal Environment 326:1-3, 1-31. [CrossRef]

13. Wen-Xiong Wang, Raymond S.K. Wong, Jingfeng Wang, Yu-fong Yen. 2004. Influences ofdifferent selenium species on the uptake and assimilation of Hg(II) and methylmercury by diatomsand green mussels. Aquatic Toxicology 68:1, 39-50. [CrossRef]

14. Steven J. Hamilton, Kathy M. Holley, Kevin J. Buhl, Fern A. Bullard, L. Ken Weston, Susan F.McDonald. 2002. Impact of selenium and other trace elements on the endangered adult razorbacksucker. Environmental Toxicology 17:4, 297-323. [CrossRef]

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y E

AST

CA

RO

LIN

A U

NIV

ER

SIT

Y o

n 08

/31/

13Fo

r pe

rson

al u

se o

nly.

15. Timothy W. Lohner, Robin J. Reash, V.Ellen Willet, Linda A. Rose. 2001. Assessment of TolerantSunfish Populations (Lepomis sp.) Inhabiting Selenium-Laden Coal Ash Effluents. Ecotoxicologyand Environmental Safety 50:3, 203-216. [CrossRef]

16. George R. Southworth, Mark J. Peterson, Michael G. Ryon. 2000. Long-term increasedbioaccumulation of mercury in largemouth bass follows reduction of waterborne selenium.Chemosphere 41:7, 1101-1105. [CrossRef]

17. Poul Bjerregaard, Beth W Andersen, J.Cliff Rankin. 1999. Retention of methyl mercury andinorganic mercury in rainbow trout Oncorhynchus mykiss (W): effect of dietary selenium. AquaticToxicology 45:2-3, 171-180. [CrossRef]

18. George R. Southworth, Mark J. Peterson, Ralph R. Turner. 1994. Changes in concentrations ofselenium and mercury in largemouth bass following elimination of fly ash discharge to a quarry.Chemosphere 29:1, 71-79. [CrossRef]

19. R.D. Handy, W.S. Penrice. 1993. The influence of high oral doses of mercuric chloride on organtoxicant concentrations and histopathology in rainbow trout, Oncorhynchus mykiss. ComparativeBiochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology 106:3, 717-724.[CrossRef]

20. John M. Besser, Timothy J. Canfield, Thomas W. La Point. 1993. Bioaccumulation of organicand inorganic selenium in a laboratory food chain. Environmental Toxicology and Chemistry 12:1,57-72. [CrossRef]

21. G.W. Bryan, W.J. Langston. 1992. Bioavailability, accumulation and effects of heavy metals insediments with special reference to United Kingdom estuaries: a review. Environmental Pollution76:2, 89-131. [CrossRef]

22. George L. Bowie, Thomas M. Grieb. 1991. A model framework for assessing the effects of seleniumon aquatic ecosystems. Water, Air, and Soil Pollution 57-58:1, 13-22. [CrossRef]

23. Ma.Lourdes A. Cuvin-Aralar, Robert W. Furness. 1991. Mercury and selenium interaction: Areview. Ecotoxicology and Environmental Safety 21:3, 348-364. [CrossRef]

24. Douglas J. Spry, James G. Wiener. 1991. Metal bioavailability and toxicity to fish in low-alkalinitylakes: A critical review. Environmental Pollution 71:2-4, 243-304. [CrossRef]

25. J. W. Parks, C. Curry, D. Romani, D. D. Russell. 1991. Young northern pike, yellow perch andcrayfish as bioindicators in a mercury contaminated watercourse. Environmental Monitoring andAssessment 16:1, 39-73. [CrossRef]

26. Ma. Lourdes A. Cuvin-Aralar, Robert W. Furness. 1990. Tissue distribution of mercury andselenium in minnows,Phoxinus phoxinus. Bulletin of Environmental Contamination and Toxicology45:5, 775-782. [CrossRef]

27. G.H Zhang, M.H Hu, Y.P Huang, P.J Harrison. 1990. Se uptake and accumulation in marinephytoplankton and transfer of se to the clam Puditapes philippnarum. Marine EnvironmentalResearch 30:3, 179-190. [CrossRef]

28. Karin Paulsson, Klas Lundbergh. 1989. The selenium method for treatment of lakes for elevatedlevels of mercury in fish. Science of The Total Environment 87-88, 495-507. [CrossRef]

29. M.L.A. Cuvin, R.W. Furness. 1988. Uptake and elimination of inorganic mercury and seleniumby minnows Phoxinus phoxinus. Aquatic Toxicology 13:3, 205-215. [CrossRef]C

an. J

. Fis

h. A

quat

. Sci

. Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

EA

ST C

AR

OL

INA

UN

IVE

RSI

TY

on

08/3

1/13

For

pers

onal

use

onl

y.

30. Richard S. Ogle, Kurt J. Maier, Peter Kiffney, Michael J. Williams, Anne Brasher, Larry A. Melton,Allen W. Knight. 1988. Bioaccumulation of Selenium in Aquatic Ecosystems. Lake and ReservoirManagement 4:2, 165-173. [CrossRef]

31. I.M. Davies, R. Russell. 1988. The influence of dissolved selenium compounds on the accumulationof inorganic and methylated mercury compounds from solution by the mussel Mytilus edulis andthe plaice Pleuronectes platessa. Science of The Total Environment 68, 197-205. [CrossRef]

32. Michael K. Saiki, T. Peter Lowe. 1987. Selenium in aquatic organisms from subsurface agriculturaldrainage water, San Joaquin Valley, California. Archives of Environmental Contamination andToxicology 16:6, 657-670. [CrossRef]

33. J. W. Parks, A. L. Hamilton. 1987. Accelerating recovery of the mercury-contaminated Wabigoon/English River system. Hydrobiologia 149:1, 159-188. [CrossRef]

34. Michael K. Saiki. 1987. Relation of length and sex to selenium concentrations in mosquitofish.Environmental Pollution 47:3, 171-186. [CrossRef]

35. David Jorgensen, J.F. Heisinger. 1987. The effects of selenium on the distribution of mercury inthe organs of the black bullhead (Ictalurus melas). Comparative Biochemistry and Physiology PartC: Comparative Pharmacology 87:1, 181-186. [CrossRef]

36. D.L. Liu, Y.P. Yang, M.H. Hu, P.J. Harrison, N.M. Price. 1987. Selenium content of marinefood chain organisms from the coast of China. Marine Environmental Research 22:2, 151-165.[CrossRef]

37. Emilien Pelletier. 1986. Mercury-selenium interactions in aquatic organisms: A review. MarineEnvironmental Research 18:2, 111-132. [CrossRef]

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y E

AST

CA

RO

LIN

A U

NIV

ER

SIT

Y o

n 08

/31/

13Fo

r pe

rson

al u

se o

nly.