Factors Controlling the Bioaccumulation of Mercury, Methylmercury, Arsenic, Selenium, and Cadmium by Freshwater Invertebrates and Fish R. P. Mason, J.-M. Laporte, S. Andres University of Maryland Center for Environmental Science, Chesapeake Biological Laboratory, P.O. Box 38, Solomons, Maryland 20688, USA Received: 19 April 1999/Accepted: 12 October 1999 Abstract. Concentrations of mercury (Hg), methylmercury (MMHg), arsenic (As), selenium (Se), and cadmium (Cd) were measured in atmospheric deposition, stream water, and biota in two streams in western Maryland. Overall, concentrations were slightly higher in the water of the lower pH Herrington Creek tributary (HRCT). Bioaccumulation factors were also higher for HRCT compared to Blacklick Run (BLK). MMHg concentra- tions in biota increased with trophic level and essentially all the Hg was as MMHg in predatory insects and insectivorous/ carnivorous fish. Thus, the overall trophic status of the organ- ism was indicated by the %MMHg in its tissues. Levels of As, Se, Cd, and Hg, however, decreased with increasing trophic level. Adsorption of As to the exoskeleton of invertebrates appears to be an important accumulation mechanism. MMHg was distributed evenly throughout crayfish and fish organs, whereas As, Se, Cd, and Hg were found in higher concentra- tions in detoxifying organs. Concentrations in biota in this study were somewhat elevated compared to other rural sites, but were less than those of point source–contaminated sites. Overall, as atmospheric inputs to the two watersheds were similar, the results of this study show the importance of water chemistry in determining the bioaccumulation of the metals and metalloids into insects. Subsequent transfer to higher trophic levels is related to both the ability of the organisms to depurate and the mode of accumulation, either directly from water or from food. Atmospheric deposition is an important source of trace metals and metalloids to remote aquatic environments and is a potential contributor to the enhanced concentrations of mercury (Hg) (US EPA 1995a, 1997) and other metals found in aquatic organisms in these systems. In addition to heightened deposi- tion, the effects of these metals may be exacerbated by the concomitant acidity of the deposition. This is especially true of the watersheds found in the Appalachian range of the eastern United States, as these forested systems receive, via long-range transport and subsequent atmospheric deposition, a significant insult of contaminants released into the atmosphere in the U.S. industrial heartland. Little is known, however, about the mechanisms controlling the transfer and bioaccumulation of trace metals and metalloids deposited into these watersheds. The sources, fate, and bioaccumulation of Hg especially as methylmercury (monomethylmercury—MMHg) has received increased attention recently (US EPA 1997; WASP 1995) as a consequence of human and wildlife concerns resulting from the consumption of fish with elevated Hg. In the United States, the EPA has targeted anthropogenic sources of Hg for regulation (US EPA 1993, 1997) to reduce inputs to the atmosphere. It is likely that future regulatory policies will focus on the other metals and metalloids, such as arsenic (As), selenium (Se), and cadmium (Cd) (US EPA 1993), that are volatilized to the atmosphere during high-temperature combustion (DOE 1996). Each element has a particular anthropogenic source inventory: (1) coal combustion and waste incineration (both medical and municipal) for Hg; (2) coal combustion for Se; (3) Cd from waste incineration; and (4) As from smelting and other indus- trial activities (Ondov et al. 1996). It has been estimated that the anthropogenic load to the atmosphere has increased total emissions by a factor of 5 for Cd, 1.6 for As, 3 for Hg, and 0.6 for Se (Nriagu and Pacyna 1988; Nriagu 1989; Mason et al. 1994). These elements are relatively strongly retained in watersheds, and human activities since industrialization has likely resulted in a dramatic increase in their burden in surface soils. This has been demonstrated for Hg (Nater and Grigal 1992; Mason et al. 1994), and it is estimated that over 90% of the Hg derived from anthropogenic sources and released to the atmosphere in the last 100 years is bound up in the terrestrial environment. This Hg is only slowly released to streams and rivers and will continue to be for a considerable period after the cessation of any anthropogenic inputs (Mason et al. 1994). Although this increase in loading to rivers is documented, we have little knowledge of the impact on metal levels in biota. More specifically, few studies have evaluated the sources, bioaccumulation, trophic transfer, and fate of metals within and across watersheds of different water chemistry. It is known that water chemistry influences the bioaccumulation of trace ele- ments into primary producers, and as this is the basis of the food chain, it ultimately determines the resultant levels in higher trophic organisms. We have previously studied the factors controlling the uptake of Hg and MMHg (Mason et al. 1994; Lawson and Mason 1998) and have extended these studies here to include the metalloids and Cd, in conjunction with a detailed examination of the distribution of these elements in higher Correspondence to: R. P. Mason Arch. Environ. Contam. Toxicol. 38, 283–297 (2000) DOI: 10.1007/s002449910038 ARCHIVESOF E nvironmental Contamination and T oxicology r 2000 Springer-Verlag NewYork Inc.
Transcript
Factors Controlling the Bioaccumulation of Mercury, Methylmercury, Arsenic,Selenium, and Cadmium by Freshwater Invertebrates and Fish
R. P. Mason, J.-M. Laporte, S. Andres
University of Maryland Center for Environmental Science, Chesapeake Biological Laboratory, P.O. Box 38, Solomons, Maryland 20688, USA
Received: 19 April 1999/Accepted: 12 October 1999
Abstract. Concentrations of mercury (Hg), methylmercury(MMHg), arsenic (As), selenium (Se), and cadmium (Cd) weremeasured in atmospheric deposition, stream water, and biota intwo streams in western Maryland. Overall, concentrations wereslightly higher in the water of the lower pH Herrington Creektributary (HRCT). Bioaccumulation factors were also higher forHRCT compared to Blacklick Run (BLK). MMHg concentra-tions in biota increased with trophic level and essentially all theHg was as MMHg in predatory insects and insectivorous/carnivorous fish. Thus, the overall trophic status of the organ-ism was indicated by the %MMHg in its tissues. Levels of As,Se, Cd, and Hg, however, decreased with increasing trophiclevel. Adsorption of As to the exoskeleton of invertebratesappears to be an important accumulation mechanism. MMHgwas distributed evenly throughout crayfish and fish organs,whereas As, Se, Cd, and Hg were found in higher concentra-tions in detoxifying organs. Concentrations in biota in this studywere somewhat elevated compared to other rural sites, but wereless than those of point source–contaminated sites. Overall, asatmospheric inputs to the two watersheds were similar, theresults of this study show the importance of water chemistry indetermining the bioaccumulation of the metals and metalloidsinto insects. Subsequent transfer to higher trophic levels isrelated to both the ability of the organisms to depurate and themode of accumulation, either directly from water or from food.
Atmospheric deposition is an important source of trace metalsand metalloids to remote aquatic environments and is apotential contributor to the enhanced concentrations of mercury(Hg) (US EPA 1995a, 1997) and other metals found in aquaticorganisms in these systems. In addition to heightened deposi-tion, the effects of these metals may be exacerbated by theconcomitant acidity of the deposition. This is especially true ofthe watersheds found in the Appalachian range of the easternUnited States, as these forested systems receive, via long-rangetransport and subsequent atmospheric deposition, a significantinsult of contaminants released into the atmosphere in the U.S.industrial heartland. Little is known, however, about the
mechanisms controlling the transfer and bioaccumulation oftrace metals and metalloids deposited into these watersheds.
The sources, fate, and bioaccumulation of Hg especially asmethylmercury (monomethylmercury—MMHg) has receivedincreased attention recently (US EPA 1997; WASP 1995) as aconsequence of human and wildlife concerns resulting from theconsumption of fish with elevated Hg. In the United States, theEPA has targeted anthropogenic sources of Hg for regulation(US EPA 1993, 1997) to reduce inputs to the atmosphere. It islikely that future regulatory policies will focus on the othermetals and metalloids, such as arsenic (As), selenium (Se), andcadmium (Cd) (US EPA 1993), that are volatilized to theatmosphere during high-temperature combustion (DOE 1996).Each element has a particular anthropogenic source inventory:(1) coal combustion and waste incineration (both medical andmunicipal) for Hg; (2) coal combustion for Se; (3) Cd fromwaste incineration; and (4) As from smelting and other indus-trial activities (Ondovet al.1996). It has been estimated that theanthropogenic load to the atmosphere has increased totalemissions by a factor of 5 for Cd, 1.6 for As, 3 for Hg, and 0.6for Se (Nriagu and Pacyna 1988; Nriagu 1989; Masonet al.1994). These elements are relatively strongly retained inwatersheds, and human activities since industrialization haslikely resulted in a dramatic increase in their burden in surfacesoils. This has been demonstrated for Hg (Nater and Grigal1992; Masonet al. 1994), and it is estimated that over 90% ofthe Hg derived from anthropogenic sources and released to theatmosphere in the last 100 years is bound up in the terrestrialenvironment. This Hg is only slowly released to streams andrivers and will continue to be for a considerable period after thecessation of any anthropogenic inputs (Masonet al.1994).
Although this increase in loading to rivers is documented, wehave little knowledge of the impact on metal levels in biota.More specifically, few studies have evaluated the sources,bioaccumulation, trophic transfer, and fate of metals within andacross watersheds of different water chemistry. It is known thatwater chemistry influences the bioaccumulation of trace ele-ments into primary producers, and as this is the basis of the foodchain, it ultimately determines the resultant levels in highertrophic organisms. We have previously studied the factorscontrolling the uptake of Hg and MMHg (Masonet al. 1994;Lawson and Mason 1998) and have extended these studies hereto include the metalloids and Cd, in conjunction with a detailedexamination of the distribution of these elements in higherCorrespondence to:R. P. Mason
EnvironmentalContaminationa n d Toxicologyr 2000 Springer-Verlag New York Inc.
organisms. The elements chosen for this study are those that aresubstantially enriched in atmospheric deposition due to anthro-pogenic emissions. Additionally, these elements are bioaccumu-lated within aquatic food chains and are potentially toxic toanimals. As no study has previously looked at sources, trans-port, and bioaccumulation in streams impacted by acidicdeposition, we set out to investigate the link between atmo-spheric deposition, watershed dynamics, and bioaccumulationof Hg, MMHg, As, Se, and Cd in biota at selected trophic levels.As the chosen western Maryland streams are remote from pointsource inputs, are forested, and do not have significant humanpresence, the dominant source of metals is atmospheric deposi-tion. Thus, these systems provide a unique environment toquantify the transfer of Hg, MMHg, As, Se, and Cd fromatmospheric deposition to fish.
Materials and Methods
Samples of insects, crayfish, and fish were collected in October 1997,April 1998, and July 1998 from two sites in western Maryland:Herrington Creek tributary (HRCT) and Blacklick Run (BLK) (Figure1). Water samples were collected monthly in both of these streamsusing appropriate ‘‘clean techniques’’ (Masonet al. 1999). They werefiltratedin situat 0.8 µm (Quartz filter, Whatman). Weekly atmosphericdeposition collections were made within the forest canopy (throughfallsamples) of both watersheds. Wet deposition collections, also weeklyintegrated, were collected at Piney Dam, which is in close proximity toboth streams (Figure 1). The Blacklick watershed (BLK) is in theSavage River State forest and is closer to Piney Dam Reservoir thanHRCT.
Stream chemistry has been monitored for a number of years in BLK,and the watershed is gauged to measure stream flow. This site has ahigh acid neutralizing capacity (ANC) and was thus chosen to berepresentative of a high pH system. The other site, HRCT, is a low pHsystem that has also been monitored and is gauged (Castro and Morgan1999). Throughfall (which includes both wet deposition and drydeposition washoff from trees) deposition collectors for Hg, metals/metalloids, and major ions were, respectively, constructed of polycar-bonate (Hg) and polyethylene (separate funnels for trace metals and formajor ions). The collectors consisted of an open funnel attached via aplastic coupling to a collection bottle—Teflon for Hg, polyethylene forother species—mounted on poles approximately 3 ft off the ground.The wet deposition collection employed an automatic MIC-B raincollector modified to allow the insertion of three funnels for thedifferent species collected: glass for Hg; polyethylene for metals andmajor ions. Details of the wet deposition collection methods are givenin Landis and Keeler (1997). The cleaning procedures and the protocolsfor collection of wet and throughfall deposition are described in detailelsewhere (Masonet al.1997a, 1997b; Castro and Morgan 1999).
Net capture was used for insects and crayfish, and fish were collectedby electroshock techniques. Samples were rinsed with distilled water,sorted into classes, and then frozen in Ziploc bags. Five insect classesand three species of fish from BLK were selected (based on feedingbehavior and genus) (Table 1). Samples from HRCT were sorted intofour insect classes and four fish species. Crayfish were found in bothstreams. When possible, samples were also divided into different age(size) classes. The differentiation was based on length for both fish andcrayfish, so these age classifications assume similar growth rates inboth streams. As the age data were used to explore bioaccumulationpatterns and not to directly compare data across streams, this approachwas valid.
Samples were transported frozen to the Chesapeake BiologicalLaboratory and were kept at215°C. Prior to analysis, samples werethawed in a laminar flow hood, and each biotic group was divided into
four subsamples; one for dry weight determination (VWR Scientificforced air oven at 60°C overnight), the others for analysis. All samples(invertebrates and fish) were analyzed as whole organisms, as opposedto measurements by others of fish that are often made on muscle tissueonly (Bloom 1992). The fish and the crayfish were crushed using amixer in order to obtain homogeneous samples. In addition, specifictissues or organs were removed from both crayfish and fish in April andJuly and analyzed to ascertain tissue distributions of the contaminantsin addition to whole body analysis. These subsamples were further splitto provide replicates when possible. Fish subsamples did not pose anyreplication limitations, but for insects, sample size was the limitingfactor and replication was not possible for subsamples with,4 insects.
Methods used for metal analysis are routinely used in our laboratoryand are similar to standard EPA methods (US EPA 1996a). For the As,Se, and Cd determinations, one aliquot of tissue was digested accordingto EPA Methods (US EPA 1996a; Keith 1991). The digestates wereanalyzed for Cd using either a Perkin-Elmer Zeeman 5000 HGA-400Graphite Furnace Atomic Absorption Spectrophotometer (GF-AAS)using standard methods (US EPA Methods, 7000 Series), or morerecently using a Hewlett-Packard 4500 Inductively Coupled Plasma-Mass Spectrometer (ICP-MS). For As and Se, samples were analyzedby hydride generation techniques using a PSA Excalibur ContinuousHydride Analyzer. The analytical techniques are similar to US EPAMethod 1632.
Samples for Hg were digested in a solution of 70% sulfuric/30%nitric acid in Teflon vials, heating overnight in an oven at 60°C (Bloomand Crecelius 1983; Masonet al.1993). The digestate was then dilutedwith distilled-deionized water and the concentration of Hg in an aliquotwas determined by cold vapor atomic fluorescence detection (CVAFS)in accordance with protocols outlined in US EPA Method 1631 (Bloomand Crecelius 1983; Bloom and Fitzgerald 1988; Masonet al. 1993).For methylmercury, samples were distilled using the technique ofHorvat et al. (1993) prior to analysis using ethylation derivitizationfollowed by isothermal gas chromatographic separation and CVAFS(Bloom 1989; Mason and Sullivan 1997). This method is routinelyused for the analysis of methylmercury in biota samples, sediments,and water.
Blanks and standards were run with each batch of samples, andsamples were not analyzed if the correlation coefficient of thecalibration curve was less than 0.99. Blank concentrations weresignificantly less than the sample concentrations for all samples.Detection limits were 0.05 ng g21 for total Hg; 0.015 ng g21 forMMHg; and ,5 ng g21 for As, Se, and Cd. Blank samples andduplicate/replicate samples and samples of standard reference materialwere also analyzed. For Hg, samples were routinely analyzed induplicate; for MMHg and the other metals, duplicates and spikeadditions were analyzed at a rate of 10% of samples. For analysis byICP-MS, relative standard deviations were always less than 5%,typically around 2%. For Hg and MMHg, standard deviations weretypically ,10%. For simplicity in presentation, these analytical errorsare not shown in figures. Error bars in figures therefore reflect thecompilation of data from different sampling sessions. Laboratory-measured values compared well with certified values for target metalsin standard reference material (SRM) (SRM 1566a oyster tissue andSRM 1646a, Estuarine Sediment, National Institute of Standard &Technology, Gaithersburg, MD, for As, Cd, and Se; SRM IAEA-142,Mussel Homogenate, International Atomic Energy Agency, Monaco,for Hg and MMHg).
Results and Discussion
Metal Concentrations in Deposition and Stream Water
The concentration of total Hg, MMHg, As, Se, and Cd wasmonitored in wet deposition at Piney Dam (Figure 1) and
284 R. P. Masonet al.
throughfall (weekly samples at both streams) and in the streams(monthly grab samples) during the duration of the biota study(Tables 2 and 3). For all the elements, there is little difference inthe average concentration in throughfall between watersheds,suggesting that the atmospheric inputs to each watershed areessentially the same. The concentrations in throughfall arehigher than that of wet deposition for all elements except Se(Table 2). Higher concentrations in throughfall suggest enhance-ment of deposition by washoff of particulate material fromleaves by wet precipitation. For Se, lower throughfall valuessuggest uptake of Se through the leaves. However, though theaverage Se value for wet deposition is higher, there is signifi-cant variability in the data and this could account for thedifferences in the averaged concentrations between throughfalland wet deposition. Other studies in western Maryland (e.g.,the
Bear Branch watershed) have found similar relative values formetals in wet compared to throughfall deposition (Churchet al.1998).
The total Hg concentration in throughfall is about 20%greater than that of wet deposition, while Cd has the highestrelative concentration (Table 3). Masonet al. (1997a; 1997b)reached a similar conclusion for Hg. As all these elements havea strong anthropogenic component and are emitted fromcombustion and other high temperature sources, the variabilitybetween elements may reflect their differences in volatility ordifferences in sources, as both factors will result in differencesin the particle size distribution in the atmosphere. The impor-tance of dry versus wet deposition is to a large degree a functionof the size distribution of particles carrying the contaminant(Ondovet al.1996).
Fig. 1. Map showing the location ofthe sampling sites (dark triangles) inGarret County, western Maryland,USA: the site of the wet depositioncollector at Piney Dam (WET) andthe stream sampling locations atBlacklick Run (BLK) and HerringtonCreek tributary (HRCT)
285Bioaccumulation Factors in Freshwater Invertebrates and Fish
The stream concentrations of the elements are similar tothose found in Maryland mountain watersheds (Churchet al.1998). Given the low particulate loading (,1 mg L21) in thesestreams under baseflow conditions (our unpublished data), thedissolved phase (,0.4 µm) is the dominant fraction, even forHg that is the most particle-reactive. The dissolved organiccarbon (DOC) concentration in the streams is also low (,1–2mg L21). The acidic HRCT appears to have higher total Hg andMMHg concentration than BLK, although the differences arenot significant (Table 2).
The MMHg concentrations in the stream are low compared tolakes and other rivers, where values are typically greater than0.1 ng · L21 (Watras and Bloom 1992). The low MMHgconcentrations in this study are likely a result of the nature ofthese streams, which do not contain significant wetlands, andwhose substrate is rocky with little sediment. Thus, there arelimited regions for methylation within the stream, given thatmethylation is mostly due to sulfate-reducing bacteria, whichare not likely active in these shallow, well-oxygenated waters,except perhaps at depth in the stream edge sediments or thesurrounding soils. Measurements of MMHg in stream water doshow a higher concentration in the lower pH HRCT and ahigher concentration in summer compared to winter, whichsuggests that bacterial control over MMHg concentration isoccurring.
The concentrations of Se are similar between streams; Cdappears to be higher in HRCT, and As is substantially higher inHRCT. The reason for the higher Cd and As concentrations inHRCT might be a reflection of the lower pH of this stream.Churchet al. (1998) found that HRCT had higher concentra-tions of Fe, Mn, Ni, Zn, and Cr, and lower Pb concentrationsthan Bear Branch, but that Cd was comparable across the
streams. Both these streams have a relatively low pH. Incomparison, metal concentrations in larger rivers (with highpH), such as the Potomac, are much lower than those found inthe acidic streams (Lawsonet al., in review). The results of thisstudy suggest that in this region, lower pH streams, even giventheir lower particulate loadings, tend to have higher metalconcentrations, as found by others (Vesely and Majer 1996).Carrollet al.(1998) concluded that of Zn, Cd, and Pb, Cd is themost mobile of the metals and its mobility is strongly influ-enced by changes in stream pH. The mobility of Cd, and to alesser degree of the other metals and metalloids, at the lower pHis likely a result of solubilization of iron oxides, and the lack ofconcomitant scavenging of metals due to carbonate precipita-tion or particulate adsorption and settling.
A comparison of the stream and throughfall concentrations(Table 3), taking into account that about 50% of the moistureinput to the watersheds is lost by evapotranspiration (Castro andMorgan 1999), illustrates that Hg is strongly retained in thewatershed, but As, Se, and Cd are more mobile. These estimatesagain reflect the higher mobility (i.e., lower retention) of As andCd in HRCT; Se appears to be similarly retained in bothstreams. These estimates are of comparable magnitude to thosemade by others for similar streams (Churchet al.1998).
Overall, the results of the deposition and stream-monitoringprogram show that, on average, the inputs to the two streams aresimilar. More detailed analysis of the data (beyond the scope ofthis paper) show differences on a smaller scale (e.g.,seasonally)and there are also differences between high and low flowperiods in the streams. Concentrations of more particulate-reactive metals, especially Hg, are elevated during storm flowcompared to base flow so the overall actual retention efficiencyis likely somewhat less than the estimated values in Table 3,which are based on monthly grab samples only. The similarityin inputs suggests that any large difference in biota concentra-tion between the two streams is likely a reflection of differencesin chemical composition and speciation in the streams.
Biota Distributions
The different organisms sampled in the two streams during thisstudy are listed in Table 1. Insects species were selectedaccording to their feeding habit as this is known to impact thebioaccumulation of Hg, and potentially the other elements. Wefound three groups of insects with a herbivorous/detritalfeeding behavior (caddisfly, mayfly, and cranefly), three othergroups were identified as predators (stonefly [2], dobsonfly, anddragonfly). The shredder stoneflies (1) that were found only atBLK were a different species from the predatory stoneflies andwere retained to allow intragenus comparison. Crayfish andbrook trout were found at both locations while the other fishspecies were found at only one location;viz., blacknose daceand sculpin at BLK; brown bullhead, creek chub, and whitesucker at HRCT (Table 1). The dissimilar distribution of fishcould result from pH differences. Indeed, while BLK shows anaverage value above 7, the pH of HRCT ranges from 5.25 to 6.7with the highest pH occurring only under low flow conditions.Species in HRCT are known to be more tolerant of acidconditions than the species found in BLK. Additionally thebrook trout found at HRCT were few compared to BLK, andthis could be linked to the fact that pH magnitude in this streamis narrower than that typical for this fish species (Eddy and
Table 1. Organisms sampled in the streams during this study. Insectsare divided as far as possible by genus and grouped according tofeeding preferences. ‘‘n’’ represents the number of sampling dateswhere the animals were found at (A) Blacklick Run and (B) HerringtonTributary
Underhill 1976; Harvey 1982; Jenkins and Burkhead 1993).Alternatively, the differences in fish community could reflectdifferences in the average water temperature and physicalcharacteristics of these streams. For example, the fish (whitesucker, creek chub, and brown bullhead) that tend to prefermore clear, cold water and lower stream flow inhabit HRCTrather than the steeper gradient, more rapidly flowing BLK,whose conditions are favored by blacknose dace.
Mercury and Methylmercury in Biota
The average concentration (X6 SD) of MMHg in insectscollected from BLK and HRCT during the three sampling dates(Oct 97, Apr 98, and July 98) are shown in Figure 2a. Overall,the concentrations of MMHg were lower in the insects fromBLK, for both predators and non-predators. Concentrationswere fairly constant over the three sampling periods (October,April, and July) as indicated by the low variability, suggestingthat the MMHg concentration in these organisms is at steadystate with that of the surroundings. The concentration ofinorganic Hg was more variable, as indicated by the largerchanges in %MMHg (Figure 2b). Differences in feeding habitswith season have been shown to affect total Hg concentration ininsects depending on whether they are predominantly feedingon algae or on detritus (Snyder and Hendricks 1995).
The trend of increasing concentration of MMHg with in-creased trophic level for insects is evident in both streams andshows similar trophic transfer factors between groups (Figure2a). This result is consistent with previous laboratory and fielddata (Watras and Bloom 1992; Masonet al.1996; Lawson andMason 1998) that has shown that although water chemistry (pH,DOC, ligand concentration) alters bioaccumulation into pri-
mary producers, there is no effect of water chemistry on themagnitude of the trophic transfer at higher trophic levels.
The insects feeding on periphyton/plant material had MMHgconcentrations that were 3–10 times those of plant materialpresent in the stream (Figure 2a), suggesting a trophic transferincrease of that magnitude. This relative augmentation issimilar to that found for various aquatic systems (Lindqvistetal. 1991; Watras and Bloom 1992; Hallet al. 1998). Similarly,though the actual food source of the various predatory insectsare not known, their concentrations are elevated above theirpotential food by a factor of 2–5. The %MMHg data show thetrend of increasing relative concentration of MMHg overinorganic Hg at higher trophic levels, with the Hg of thepredatory insects being, for the most part, all MMHg (Figure2b). The genus of the insect seems to have little effectscompared to the feeding behavior. Indeed, the comparisonbetween the two species of plecoptera (stonefly 1 and 2)indicates that accumulation is 8.5 higher for the insectivorousspecies than for the herbivorous species.
The crayfish in both BLK (Figure 3a) and HRCT (Figure 4a)have concentrations of MMHg that are lower than that of thecorresponding predatory insects (Figure 2a) but higher than thatof the other insect groups. This intermediate concentrationreflects the more generalist feeding strategy of the crayfish(omnivore). The differences in trophic status are also evidentwhen average bioaccumulation factors (BAFs) are calculated.The BAF of the crayfish is intermediate between that ofpredatory and nonpredatory insects (Figure 5). Because of thehigher MMHg body burdens for similar organisms in HRCTcompared to BLK, the BAF values are somewhat higher forHRCT where the same species are being compared. A numberof studies have demonstrated that MMHg bioaccumulation ishigher in lower pH aquatic systems (e.g.,the Little Rock Lakestudy; Watras and Bloom 1992). A number of hypotheses havebeen put forward to explain this phenomenon in terms of theinfluence of pH (and other parameters) on water columnspeciation (Masonet al. 1996; Haineset al. 1995; Griebet al.1990; Langeet al.1993; Bodalyet al.1993) and, as a result, onbioaccumulation into primary producers. Experimental studieson the Turkish crayfish (Astacus leptodactilus) indicate that thepH tend to modify MMHg direct uptake by changing mercuryspeciation rather than by affecting the physiology of animals(Laporteet al.1996). Overall, the BAF values in this study aresimilar to those found for organisms occupying a similartrophic status in Lake Michigan (Mason and Sullivan 1997);Little Rock Lake, Wisconsin (Watras and Bloom 1992).
Interestingly, the concentrations of MMHg in the small troutfrom each stream are relatively low compared to the larger trout(Figures 3a and 4a), and in BLK there is a concomitant decreasein the %MMHg in smaller fish (Figure 3b). While the lower
Table 2. Concentration of mercury (Hg), methylmercury (MMHg), arsenic (As), selenium (Se), and cadmium (Cd) in wet deposition, throughfall,and stream water for the two watersheds (all concentrations in ng · L21)
Table 3. Relative throughfall concentrations, relative streamconcentrations and retention efficiency of the watersheds for eachmetal based on the data in Table 2
* Thru/Wet 5 throughfall/wet deposition; Strm/Thru5 stream/throughfall; %Ret5 percent retained** Percent retained is estimated based on the assumption that 50% ofthe water input is lost via evapotranspiration
287Bioaccumulation Factors in Freshwater Invertebrates and Fish
BAF is a reflection to some extent of the continual concentra-tion increase of MMHg with age due to its bioaccumulativenature (see below), the lower %MMHg in the small trout fromBLK might reflect as well a difference in the feeding behaviorof these fish. Additionally, in both streams, the BAF for smalltrout is less than that for the other insectivores (dace and suckerin Figure 5a). Brook trout are insectivores generally, andpreliminary gut analysis suggests a dominance of mayflies,which are herbivorous insects. This would therefore put themon the same trophic level as predatory insects. The relative BAFvalues reflect this to some extent. In addition, comparison ofconcentrations in trout from BLK for three different age classes(Figure 6) further demonstrates that the trout are changingfeeding habits with age as there is a continued increase in%MMHg (Figure 6c), as well as an increase in MMHgconcentration (Figure 6b). Brook trout are known to shift theirdiet from predominantly insect to insect plus small fish with age
(Eddy and Underhill 1976; Jenkins and Burkhead 1993), whichis consistent with our MMHg data. Age 1 trout (,100 mm) hadabout 60% MMHg, similar to that of crayfish, while all the Hgin age 3 trout was MMHg. In contrast, the change in %MMHgwith size is less evident for crayfish, varying between 60% and80% with only a small increase with age (Figure 7b), which isconsistent with their lack of marked change in food preferencewith age. The creek chub also shifts from insects to feeding onsmall fish with age, but due to the limited number of smallversus large fish, we are unable to show size-related data forcreek chub.
The concentrations of MMHg in the fish are relatively lowcompared to the value set by federal consumption guidelines(1,000 ng · g21 wet weight (WW); US EPA 1995a, 1997). Somestates in the United States have set limits of 500 ng · g21 or less(Minnesota; MPCA 1994), and in terms of these guidelines, theconcentrations in the HRCT fish are of concern given the fact
Fig. 2. The concentration of (a) methyl-mercury (MMHg) and (b) the percent ofthe total mercury as methylmercury(%MMHg), the concentrations of (c)arsenic (As), (d) cadmium (Cd), and (e)selenium (Se) in plant tissue and insectsfrom Blacklick Run (BLK) and Herring-ton Creek tributary (HRCT). Averagevalue of the concentrations measured onthe three sampling occasions (October1997, April 1998, and July 1998)(X 6 SD, n5 see Table 1). All concen-trations in ng · g21 wet weight of wholeindividuals. Peri5 periphyton; Bryo5bryophytes; CraneF5 cranefly; Cad-disF5 caddisfly; MayF5 mayfly; Sto-neF 15 shredder stonefly; StoneF25predatory stonefly; DragonF5 dragon-fly; DobsonF5 dobsonfly. See Table 1
288 R. P. Masonet al.
that these fish were generally less than 15 cm in length. Ifsimilar conditions existed in a larger stream where fish wouldattain a larger size, it is possible that the MMHg concentrationwould exceed consumption guidelines. This is shown bycomparison of our data with those of freshwater systems inMaine (Stafford and Haines 1997) where size-related concentra-tions for brook trout have been documented. Indeed, the authorsobtain for similarly sized trout (10–20 cm) results that arecomparable to those observed in our study (respectively,20–200 ng · g21 and 20–60 ng · g21, WW). Their values for fish.30 cm reach or exceed the limits fixed by the EPA, and thesame trend can be expected in fish from Maryland streams.
Arsenic, Cadmium, and Selenium in Biota
Insect: Figures 2c–2e show the concentrations of As, Cd, andSe in insects. In this study, As and Cd stream concentrationswere higher for HRCT than BLK (Table 2), but there is noconcomitant variation in insect concentration (Figure 2c, 2d).
This lack of difference could be explained by the highvariability of the results for As, Cd, and Se, which derive in partfrom the elevated As and Se concentrations in the herbivores/detritivores in July and October. However, these variationswere not systematic, and we could not conclude that there was aseasonal effect on the concentrations. Overall, our results showthat As, Cd, and Se concentrations in organisms tend todecrease with increasing trophic level.
Arsenic concentrations found in the insects in our study (bothBLK and HRCT) are similar or higher than those found at otheruncontaminated sites, but less than that found at contaminatedsites, such as the Clark Fork River Superfund site. Arsenicconcentrations in different insects at the Clark Fork River werefound to be around 750 ng · g21 WW (5 ppm DW) forPlecoptera, 600–7,500 for Tricoptera, and 6,000–10,000 ng · g21
for Ephemeroptera (Cainet al. 1992). At a nearby referencesite, concentrations were, respectively, around 300, 200–1,050,and 1,500–2,400 ng · g21. Those values are comparable to theresults of our study (see Figure 2c). Cainet al. (1992) found astrong log-log relationship between As concentration and insect
Fig. 3. The concentration of (a) methyl-mercury (MMHg), (b) the percent of thetotal mercury as methylmercury(%MMHg), the concentrations of (c) ar-senic (As), (d) cadmium (Cd), and (e) sele-nium (Se) in crayfish and fish from Black-lick Run on the three sampling occasions(October 1997, April 1998, and July1998). All concentrations in ng · g21 wetweight of whole individuals. Crayfish,Sculpin, Dace5 blacknose dace,SmTrout5 small brook trout, LgTrout5large brook trout. See Table 1
289Bioaccumulation Factors in Freshwater Invertebrates and Fish
weight that appeared not to be dependent of insect taxa orfeeding preference, but to be more site-related, with thebioaccumulation decreasing with declining sediment load. Thisrelation between the size and accumulation for small insectsreflects dependence on the surface/volume ratio during theprocess of adsorption directly from water. Corroborating thisidea, the herbivore insects show an increase of the concentra-tion with decreasing average size of the organism: cranefly (300mg) , caddisfly (25 mg), mayfly (20 mg). Because theseorganisms are not strictly comparable since they differ by theirgenus, their behavior, and other factors, we present a compari-son of concentration versus size (Figure 8) for mayflies asillustrative of the importance of insect size in determiningconcentration. This is especially true for As and Se, and to alesser degree for inorganic Hg. There was no strong trend forMMHg, consistent with the notion that all the MMHg is comingfrom uptake from food. There was no strong evidence of trophictransfer of As since concentrations of this metalloid weresimilar in periphyton, bryophytes, and insects. A study by Hareet al. (1991) found that As was mostly accumulated externally,in agreement with Cainet al.(1992). The amount of adsorptionis probably a function of pH, which varies seasonally within thestreams, especially HRCT (Castro and Morgan 1999).
Cd stream concentrations are higher for HRCT than BLK(Table 2) but there is not a similar difference in insectconcentration (Figure 2d). The values (from 100 to 400 ngCd · g21, WW) are high compared to what Cainet al. (1992)found at the background site (15–60 ng g21 WW) and similar orless compared to 150–450 ng g21 WW at the contaminatedClark Fork River sites. The concentrations in the smaller insectsappeared higher in that study in contrast to this work (Figure 9).There is still no real consensus on the influence of the size onCd accumulation. However, the results suggest that Cd adsorp-tion to the exoskeleton is low compared to the uptake across therespiratory or the trophic barriers. The free ion Cd21 is usuallyconsidered the most bioavailable form and is taken up acrossgills through transport systems initially designed for Ca (Ver-bostet al.1989; Thomannet al.1997; Craiget al.1999). Hareand Tessier (1998) relate Cd concentrations inChaoborusto thefree metal ion concentration in water, as influenced by the pH ofthe system. Nevertheless, Cd availability can be stronglydecreased when ligands such as chloride (in sea water) orsuspended matter are abundant in the water column. Underthese conditions, the trophic contamination can become preva-lent, as Fisher and Reinfelder (1995) concluded it in a review ofthe marine invertebrate literature. In addition, a study by Hare
Fig. 4. The concentration of (a) methylmer-cury (MMHg), (b) the percent of the total mer-cury as methylmercury (%MMHg), the con-centrations of (c) arsenic (As), (d) cadmium(Cd), and (e) selenium (Se) in crayfish and fishfrom Herrington Creek Tributary on the threesampling occasions (October 1997, April 1998,and July 1998). All concentrations in ng · g21
wet weight of whole individuals. Crayfish,Bullhd 5 brown bullhead, Sucker5 whitesucker, SmTrout5 small brook trout,LgTrout5 large brook trout, Chub5 creekchub. See Table 1
290 R. P. Masonet al.
et al. (1991) identified the gut as the primary site of Cdaccumulation. Cainet al. (1992) noted a relationship betweensediment Cd concentration and insect concentration, but nostrong concentration change with size, season, or feedingbehavior was observed at the Clark Fork River sites. Our resultsare in general agreement with all these observations. Given thelow particulate loading in these two streams (,1 mg · L21)dissolved Cd exists primarily as Cd21 and pH has littleinfluence on the chemical speciation. It is likely that organismstake Cd from both surrounding water and food, but we cannotconclude the dominant uptake mechanisms for Cd into insectsfrom this study. Because of the higher concentrations measuredin the herbivore group compared to the predatory insects, itseems that the trophic assimilation of Cd contained in theinsects is lower than that of Cd linked to the plants (periphytonor macrophytes). Depuration is likely an important loss mecha-
nism for Cd and the metalloids. Lindqvistet al. (1995) found arapid loss of Cd (and inorganic Hg) from a predatory beetleafter feeding with a contaminated diet. Interestingly, MMHgwas strongly retained with less than 40% loss after a month ofdepuration. The rate of depuration also differs with the consid-ered organism. For example, Inzaet al. (1998) demonstrated amuch slower decontamination of Cd and Hg in clams after theinitial exposure (MMHg was again strongly retained). Theseresults suggest that the relatively low BAFs found for As, Se,Cd, and inorganic Hg compared to MMHg (Figure 6) might bepartially related to the ability of the organisms to regulate anddepurate these elements.
There is little data for Se in insects in the literature. In thecontaminated San Joaquin river in California, Saikiet al.(1993)found Se concentrations in the water around 25 µg · L21,invertebrates had 14,000 ng Se · g21, and fish 17,000 ng · g21,giving BAFs (wet basis) of around 560 for invertebrates. In ourstudy, BAF values ranged from 0.2 to 63 104 and concentra-tions in invertebrates ranged from 200 to 2,000 ng · g21 (Figure2e). Our BAFs values were much higher and suggest that thereis some regulation of Se accumulation in the San Joaquin.Alternatively, normalization to water concentration may notaccurately predict bioaccumulation. Other investigators havereached similar conclusions and suggest that sediment concen-tration, normalized to organic content, is a better predictor of Seuptake and toxicity than water concentration (Canton and VanDerveer 1997; Van Derveer and Canton 1997). Studies withmarine organisms have shown no discernible difference be-tween planktivorous and carnivorous species in Se concentra-tion. However, Reinfelder and Fisher (1991) found very highassimilation efficiencies for Se by copepods feeding on algae,and Fisher and Reinfelder (1995) suggest that food is thedominant source of Se to marine organisms. A laboratory studyof Se food chain accumulation showed that the chemical formof the Se influenced its rate of accumulation into algae andsubsequently into daphnids and bluegills (Besseret al. 1993).Organo-Se was most efficiently bioaccumulated, and accumula-tion from food appeared to be more important than uptake fromwater. Concentration factors for the higher trophic levels (algaeto daphnids; daphnids to fish) were between 0.5 and 1,suggesting no net accumulation, on a per weight basis, abovethe algae. Depuration of Se by bluegill was relatively rapid,with about 50% or more of the accumulated Se lost within amonth (Besseret al.1993). This rate is similar to that of As andCd, as discussed above. Our results show similar trends to thisstudy in terms of accumulation and trophic transfer for insects.
Crayfish and Fish: Arsenic and Se concentrations in crayfishand fish varied between streams in a similar manner to thevariability observed in stream water concentration (Table 2;Figures 3 and 4). As a result, the bioaccumulation factors aresimilar for representative organisms of each trophic level(Figure 5). The major difference is for Cd, where the BAF isabout 0.5 log units smaller in BLK compared to HCRT. Thus, itappears that the lower pH in HRCT (or another factor) isleading to a slightly increased Cd uptake into fish either bycontrolling directly the metal chemical speciation or by modify-ing the fish metabolism. The concentrations of As, Se, and Cd inthis study are lower in crayfish and fish than in the herbivorous
Fig. 5. (a) Bioaccumulation factors for methylmercury for selectedspecies of insects, crayfish, and fish for both streams. CaddisF5caddisfly, StoneF 25 predatory stonefly, Crayfish, Dace/Sucker5Blacknose dace or white sucker, depending on stream, SmTrout5small trout and LgTrout5 large trout; (b) Bioaccumulation factors forsmall brook trout for methylmercury (MMHg), inorganic mercury(InorgHg), arsenic (As), cadmium (Cd), and selenium (Se) for April1998
291Bioaccumulation Factors in Freshwater Invertebrates and Fish
insects (Figures 2–4). There is no indication of a strongdifference in concentration between fish species.
The increase in concentration with age, seen for MMHg forboth fish and crayfish (Figures 6 and 7), is less clear for theother metals. It appears that As is relatively constant with age inBLK crayfish, but increases with age in HRCT crayfish (Figure7b). Based on the similarity in %MMHg in these crayfish withage (Figure 7e) we suggest that there is not a strong shift in dietwith age for crayfish, so other causes must account for theobserved changes with age for As and the lack of consistencybetween streams. Adsorption to the carapace has been sug-gested as an important accumulation mechanism for As forinsects (Cainet al. 1992), and the same appears to be true forcrayfish (see below—Distribution between organs). Because ofthe significant participation of the carapace in the total accumu-lation measured in crayfish, the molt events can lead to asubstantial decontamination of As, and this could account forthe heterogeneity of the results. For trout, there is little changein As with age in July, and concentrations are lower than thosefound in April. Adsorption cannot account for these differences.
As the concentration of As in trout is lower than in crayfish(Figures 3, 4, 6, and 7), especially in summer, it is apparent thatAs in higher organisms is readily excreted, and hence there is noconsistent value between seasons as there is for MMHg. As the
major bioaccumulation transfer for As occurs between waterand algae, the concentration and food source at the base of thefood chain has a strong impact on the resultant concentration infish.
For Cd, the crayfish results are somewhat contradictory andvariable. This may reflect adsorption to the carapace or otherfactors. Fish, however, show some increase with age. However,the trout concentrations are lower than the crayfish, suggestingthat although there is no net bioaccumulation, there is storage ofCd in the trout such that there is an age-related effect. For Se,there is little difference in bioaccumulation with the age of thecrayfish (Figure 7). It is not the case for the fish that show anincrease of a factor of two in July and less of a trend in April(Figure 6). This may reflect storage of Se in proteins, as it isknown that higher organisms have requirements for Se (Sasakuraand Suzuki 1998). It has been suggested that Se can reduce thetoxicity of Hg and that marine mammals and large fish can storeHg in association with Se (Kaiet al.1995). Doreaet al. (1998)found a positive correlation between Hg and Se in fish from theHg-contaminated Madeira River and found a higher molar ratio(Hg:Se) in piscivorous compared to herbivorous fish. Thedifferences in the concentration patterns of Se, Hg and MMHgbetween organs in our study do not, however, suggest that this isoccurring in the trout.
Fig. 6. The (a) average fish length and (b) concentration ofmethylmercury (MMHg), (c) the percent of the total mer-cury as methylmercury (%MMHg), the concentrations of(d) arsenic (As), (e) cadmium (Cd), and (f) selenium (Se) inbrook trout from Blacklick Run according to size. Age1:,100 mm fish, Age2: 100–200 mm fish, and Age3:.200mm fish. Samples from both April and July 1998 shown
292 R. P. Masonet al.
The study of bioaccumulation as a function of the size (andthus of the age) does not only reflect the exposure time, but isthe integration of many parameters, such as the variations incontamination pressure, growth rate (which could lead togrowth dilution), or the change of diet. Net accumulationmeasured in organisms results from equilibrium between up-
take and elimination rates as well as storage capacities. Therewill be no net bioaccumulation of an element if its trophictransfer is less than that for carbon;i.e., relative to carbon(tissue mass), the concentration will decrease with increasingtrophic level. However, these organisms could still bioconcen-trate the element with age if there is not a significant depurationroute; i.e., uptake rate exceeds loss by growth dilution anddepuration. If net bioaccumulation occurs with each trophiclevel, then insectivorous/carnivorous fish should have thehighest concentrations. This is clearly not so for As, andseasonal differences suggest that As is efficiently depurated, asdiscussed above. The same is true for Se and Cd, as there are noclear trends across trophic levels.
Metal Distribution Between Organs
The distributions of the metals and metalloids in the organs oftrout and crayfish for the sampling campaign of April 1998 areshown in Figures 9 and 10. In trout, MMHg is relatively evenlydistributed on a concentration basis, and this is expected giventhat MMHg is mostly bound in protein via association withthiol groups. MMHg concentrations are always higher in organsof fish from HRCT. In contrast, inorganic Hg is mostlyconcentrated in the detoxifying organs (liver, kidney) ratherthan in muscle. The concentration of MMHg in gills iscomparable to the other organs, indicating that while directuptake from water via the gills may be occurring, it is either notthe dominant uptake route or that MMHg is rapidly transferredand distributed to internal organs. Even given the DOCconcentrations in these streams (about 1 mg L21; our unpub-lished data), and because of the low chloride concentrations(about 30 µM; Castro and Morgan 1999), most of the MMHg(and also most of the inorganic Hg) will be bound to organicmatter in the water column. This conclusion is based onthermodynamic equilibrium estimations using literature valuesfor the various equilibrium constants (Dyrssen and Wedborg1991; Hudsonet al. 1994; Masonet al. 1996; Stumm andMorgan 1996). In addition, organic complexation would beenhanced in the higher pH BLK stream. Overall, direct uptakeacross the gills will be hindered by organic complexation,compared to that expected if MMHg was bound to inorganicligands (Leaner, personal communication), but the higherMMHg and inorganic Hg concentrations in gills of fish fromHRCT compared to BLK is consistent with the expectedspeciation of MMHg and Hg in the two streams. These resultsconfirm the belief that MMHg accumulation occurs primarilyfrom food for fish, as well as for the invertebrates. Theconcentration of MMHg in the fish is greater than that of thefood (stomach contents; Figure 9), as expected for MMHg as itis strongly bioaccumulated.
The relative concentrations in all organs are comparablebetween streams, except for the intestine where a very highMMHg concentration was found for HRCT and a very lowconcentration for BLK (Figure 9). The high HRCT concentra-tion corresponds to a low inorganic Hg concentration in theintestine. It is likely that the concentration of MMHg and theother metals and metalloids in the intestine varies according towhether the fish has been actively feeding or not. For the brain,the low MMHg concentration compared to the other organs,and the relatively high inorganic Hg concentration, suggests the
Fig. 7. The concentration of (a) methylmercury (MMHg) and (b) thepercent of the total mercury as methylmercury (%MMHg), theconcentrations of (c) arsenic (As), (d) cadmium (Cd), and (e) selenium(Se) in crayfish from both streams in April 1998, according to size.Size1:,2.5 cm, Size2: 2.5–5 cm, Size3:.5 cm
Fig. 8. The concentration of arsenic (As), selenium (Se), and inorganicmercury (Hg) in mayflies showing the effect of size on concentration.Data from both streams are pooled
293Bioaccumulation Factors in Freshwater Invertebrates and Fish
possibility that the MMHg is being excluded from the brainrelative to inorganic Hg as it has been shown to occur inmammals (Magos 1997). It is also possible that demethylationis taking place in the brain (Mottetet al.1997). In the crayfish,there is a strong accumulation of inorganic Hg in the gills andcarapace (Figure 9). The concentration of inorganic Hg in thecarapace is higher than that of the muscle, while it is the exactopposite of MMHg. Clearly, Hg and MMHg are taken up,transferred, and stored differently in both crayfish and trout.The high carapace concentration of inorganic Hg and relativelyhigh gill inorganic Hg in the crayfish is more apparent ascrayfish occupy a lower trophic level; therefore food uptake ofMMHg and inorganic Hg is less dominant given the lowerconcentrations in the food.
The metalloids are mostly concentrated in the liver andkidneys (Figures 9 and 10), which is expected since they areactively eliminated by the organisms. Arsenic concentrationsare also high in the carapace of the crayfish and the remainderof the trout (mostly skin and bones), confirming the particularbehavior of As, which is mainly adsorbed on external layers.For the crayfish, Cd appears to be strongly accumulated in thegills, suggesting that direct uptake is occurring and that thisorgan shows a strong ability to act as a barrier able to retain themetal entering via this contamination route. The results are
equivocal for fish, although gill concentrations are higher thanthose of the whole body for Cd in fish (Figure 9). Muscleconcentrations of As, Cd, and Se are in general much lowerrelative to the other organs, with the exception of Se in themuscle of the crayfish (Figure 9 and 10).
Selenium is strongly bioconcentrated in kidney, liver, andgills for fish, and in the hepatopancreas of the crayfish, but notin crayfish gills. The differences in gill concentrations betweenorganisms suggest that direct uptake from water is not occur-ring, as it would be expected to be similar between species.Accumulation of As via the gills is also not indicated by thedata. Overall, the distributions in the various organs for As, Se,and Cd are similar to that expected for each element based ontheir known chemistry and route of uptake.
In summary, the distribution of Hg, MMHg, As, Se, and Cd inthe organs of fish and crayfish reinforce the accepted notionsconcerning the routes of accumulation. Accumulation fromfood is the dominate uptake mechanism for MMHg and Se.Uptake via the gills appears to be important for Cd, and to alesser extent for inorganic Hg. Both inorganic Hg and As aretaken up in the carapace of the crayfish. It is expected that thedistribution and accumulation pathways identified for crayfishare also applicable to the insects.
Fig. 9. The concentrations of (a) methylmercury(MMHg), (b) inorganic mercury (Inorg Hg), (c) arsenic(As), (d) cadmium (Cd), and (e) selenium (Se) in troutorgans for fish collected in April 1998
294 R. P. Masonet al.
Acknowledgments.We thank our colleagues at Versar and the Appala-chian Laboratory, University of Maryland Center for EnvironmentalScience, for their assistance in sample collection and identification. Wethank the Maryland Department of Natural Resources Power PlantTopical Research Program for supporting this work through grant#CB95-009-002 and through a subcontract under Versar’s BiologyIntegrator Contract with DNR. We also thank Brenda Yates formanuscript preparation. Contribution No. 3260, University of Mary-land Center for Environmental Science.
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297Bioaccumulation Factors in Freshwater Invertebrates and Fish
