Ž .The Science of the Total Environment 229 1999 1]19

Review article

Bioaccumulation of heavy metals by aquaticmacro-invertebrates of different feeding guilds:

a review

K.L. Goodyeara, S. McNeillb,U

aApplied Geochemistry Research Group, Royal School of Mines, Imperial College, South Kensington, London, SW7 2BP,UK

bNorth Block, Biology Department, Silwood Park, Imperial College, Ascot, Berkshire, SL5 7PY, UK

Received 11 July 1998; accepted 10 February 1999

Abstract

The available literature on heavy metal bioaccumulation by freshwater macro-invertebrates has been analysed. Avery uneven data distribution was found. Ephemeroptera and Diptera are the most commonly investigated orders ofinsect larvae, whilst many orders are not represented at all. The collector]gatherer and predator feeding guilds aremore frequently investigated than other guilds. Furthermore, Zn, Cu, Pb and Cd are the most intensively researchedheavy metals, and only infrequent investigations of other metals are documented. Relationships between metalconcentrations in the animals and levels in sediments and waters were determined from the pooled data for threefeeding guilds. No one relationship represents how each metal interacts within the feeding guilds. Each of the four

Ž .metals Zn, Cu, Pb and Cd displays a unique relationship between metal concentrations in sediments or waters withthose in individual feeding guilds of macro-invertebrates, indicating the relative importance of different sources ofmetals to the different feeding types. Biomagnification of Zn, Cu, Pb and Cd has been demonstrated not to occurbetween these guilds. Q 1999 Elsevier Science B.V. All rights reserved.

Keywords: Bioaccumulation; Heavy metals; Aquatic macro-invertebrates; Feeding guilds

1. Introduction

Bioaccumulation of heavy metals by aquaticorganisms is a reasonably well documented field

U Corresponding author.

of research. The majority of such investigationshave been undertaken since the 1970s at an in-creasing rate. There is, however, still a limitedamount of information about the biology of trace

Žmetals in freshwater organisms Hare, 1992,.Rainbow and Dallinger, 1992 , or their effects on

Ž .freshwater ecosystems Gower et al., 1994 . Fur-

0048-9697r99r$ - see front matter Q 1999 Elsevier Science B.V. All rights reserved.Ž .PII: S 0 0 4 8 - 9 6 9 7 9 9 0 0 0 5 1 - 0

( )K.L. Goodyear, S. McNeill r The Science of the Total En¨ironment 229 1999 1]192

thermore, it has been noted that ‘to date, insectshave been used to a limited extent in the study of

Žmetal contamination in freshwater’ Hare and.Campbell, 1992 .

Ž .Hare 1992 provided a succinct summary ofmany of the reasons which make insect larvaeattractive as biomonitors, and other authors, in-

Ž .cluding Myslinski and Ginsburg 1977 , Lynch etŽ . Ž .al. 1988 and Hare and Campbell 1992 offered

further reasons for their use in biomonitoring.These reasons are listed below:

1. a common and diverse group of animals whichare found in freshwater of all types;

2. many taxa are fairly sedentary and thus rep-resentative of local conditions;

3. many taxa are benthic and thus are closelyassociated with sediments;

4. they may accumulate metals and yet toleratelow]moderate metal concentrations;

5. metal concentrations in the animals appear tobe related to those in their environment;

6. a life-span of several months]years allowsintegration of contaminants into their bodiesover a reasonable period of time, but not solong that it avoids short-term changes in theenvironment;

7. since most are the immature stages of thelife-cycle, body concentrations are not af-fected by reproductive cycles or sexual dif-ferences;

8. they are near the base of foodchains, so maybe vital agents of metal entry into foodchains.

Aquatic macro-invertebrates therefore appearto have the potential to be useful biomonitors inthe future, despite the limited interest shown inthem to date. The aim of this investigation is toreview the available literature and to determineto what extent there is a good relationship

Ž . Ž .between trophic types guilds Root, 1973 ofmacro-invertebrates and the metals in their envi-ronment.

2. Methods

Previous investigations concerning freshwatercontamination and macro-invertebrates are

largely confined to community structure studies.Information from the literature was pooled, re-gardless of its nature; i.e. field or laboratory based,geographical location, metals investigated, etc. Adetailed summary of these papers is presented inAppendix A.

The data were split into five categories basedon feeding guild. The feeding guilds chosen arelisted below, with the definitions taken from Be-

Ž .gon et al. 1990 :

Ž .1. Collector]Gatherer C-G , animal whichgathers small particles of organic materialfrom the sediments;

Ž .2. Scraper]Grazer S-G , animal which grazersthe organic layer of algae, micro-organismsand films on stones and other substrates;

Ž .3. Predator Pr , animal which consumes otherorganisms;

Ž .4. Shredder Sh , animal which feeds on coarseparticles of organic matter;

Ž .5. Filterer Fi , animal which feeds on minuteparticles of suspended in water, which arestrained through mucus or a meshwork oflamellae.

The animals in each of these categories arepresented in Table 1. Common names are alsogiven for the orders as most species do not havecommon names. The data were then investigatedfor relationships between metal concentrations inthe animals and those in the environment for arange of metals within guilds and for each metalbetween guilds. Data were plotted against waterand sediment heavy metal concentrations in bothcases. For each relationship, the r-value was cal-culated and regression analysis performed.

3. Results

3.1. Range of data a¨ailable

Visual inspection of the data revealed somerelevant observations of the distribution of thedata within the literature.

The metals investigated were wide ranging, butthe majority of studies focused on four metals:Zn, Cu, Pb and Cd. The former two of these are

( )K.L. Goodyear, S. McNeill r The Science of the Total En¨ironment 229 1999 1]19 3

Table 1The invertebrates in each feeding guild of the present review. Data are taken from the literature, and the references are listed inAppendix A

Collector]gatherer Scraper]grazer Predator Shredder FiltererŽ . Ž . Ž . Ž . Ž .C-G S-G Pr Sh Fi

Hexagenia sp. Campeloma sp. Placobdella sp. Gammarus sp. SphaeriumHexagenia limbata Gnoibasis sp. Haemopsis sp. Gammarus pulex Orconectes sp.Ephemera danica Pleurocera sp. Erpobdella sp. Elliptio complanataEphemera ¨ulgata Limnaea sp. Erpobdella octoculata Fusconaia fla¨aPotamanthus sp. Physa sp. Agridae Amblema plicataEcdyonurus ¨enosus Asellus sp. Argia sp. Quadrula quadrulaStenonema sp. Asellus aquaticus Brachyptera risiRithrogena sp. Asellus meridanius Amphinemura sulcicolisEphemerella grandis Leuctra sp.Ephemerella ignita Classenia subulosaLeptophlebia ¨espertina Hesperoperla pacificaBaetis sp. Perla bipunctataBaetis ¨ernus Pteronarcys californicaBaetis rhodani Pteronarcella badiaArctopsyche grandis Isognoides sp.Hydropsyche sp. Skwala americanaHydropsyche pellucidula Isoperla grammaticaHydropsyche angustipennis Perloides microcephelaBrachycentrus sp. Chloroperla sp.Phryganea sp. Sigara sp.Cheumatopsyche sp. Sialis sp.Limnephilidae Rhyacophila nubilaLimnephilus sp. Rhyacophila dorsalisPotamophylax latipennis Polycentropus fla¨omaculatusTipula sp. Plectrocnemia conspersaSimulium sp. Chaoborus punctipennisChironomidae Procladius sp.Chironomus riparius Dytiscus sp.Glyptotendipes sp. Oreodytes sanmarki

Limnius ¨olckmari

Žknown to be essential elements Dadd, 1973;.Bowen, 1979; Kelly, 1988; Hopkin 1989 , whilst

the latter two metals are not known to be essen-Žtial or beneficial to living organisms Keenan and

.Alikhan, 1991 . A series of other metals weredetermined less frequently, i.e. Hg, Ni, Al, Fe,Mn, As, Cr, whilst a very sparse amount of data

Žexisted for Co, Mo, Sb, Li, Na, Ca see Appendix.A .A wide range of macro-invertebrates have been

Žused in bioaccumulation investigations Appendix.A . It is unusual that more than one investigation

has studied the same species or genus of animal.Therefore to draw comparisons between data in

the literature is difficult, unless broad groups oforganisms are used. Several taxonomic groupshave been used more frequently than others. Asummary was made of the numbers of investiga-tions undertaken on each order and family ofmacro-invertebrate, and is presented in Table 2.For example, the orders Diptera and Ephem-eroptera have been previously investigated on

Žmany occasions 38 and 33 investigations, respec-.tively , whilst Odonata and Decapoda have a

Žsparse previous literature five and one investiga-.tions, respectively .

The numbers of field- and laboratory-basedinvestigations are not equal; the field investiga-

( )K.L. Goodyear, S. McNeill r The Science of the Total En¨ironment 229 1999 1]194

Table 2The number of biogeochemical investigations which have been undertaken on various aquatic macro-invertebrate orders and

afamilies

Order Family Number Order Family Number

Amphipoda 6 Hemiptera 2Ž . Ž .sandhoppers Gammaridae 6 bugs Corixidae 2

Isopoda 8 Megaloptera 3Ž . Ž .woodlice Asellidae 8 alderflies Sialidae 3

Decapoda 1 Neuroptera 1Ž . Ž .crayfish Astacidae 1 lacewings 32

Ephemeroptera 33 Trichoptera 32Ž . Ž .mayflies Ephemeridae 12 caddisflies Rhyacophilidae 3

Potamanthidae 1 Polycentropidae 1Ecdyonuridae 6 Hydropsychidae 16Ephemerellidae 6 Bracycentridae 4Leptophlebidae 1 Phryganeidae 3Baetidae 6 Limnephelidae 4

Odonata 5 Leptoceridae 1Ž .dragonflies Aeshnidae 1 Diptera 39

Ž .Agriidae 3 true flies Tipulidae 4Plecoptera 25 Chaoboridae 2Ž .stoneflies Taenopterygidae 1 Simulidae 4

Nemouridae 1 Chironomidae 24Leuctridae 1 Phagionidae 1Perlidae 5 Coleoptera 4

Ž .Pteronarcidae 8 beetles Dytiscidae 2Perlodidae 7 Elminthidae 1Chloroperlidae 1

aAttention is drawn to the unequal distribution between the orders and families.

tions far out numbering the laboratory ones. It isnot clear why this should be so, as each type ofstudy complements the other. Both field- andlaboratory-based investigations are imperative ifbioaccumulation models are to be constructedand utilised in biomonitoring or environmentalimpact studies. It was also noted that a smallerselection of invertebrate groups have been stud-ied in the laboratory than in the field.

There is also an uneven distribution of investi-gations into the biogeochemistry of each of thefive feeding guilds listed above. The guilds of

Ž . Ž .collector]gatherer C-G , scraper]grazer S-GŽ .and predator Pr have been more intensely inves-

tigated, whilst the shredder and filterer guildshave a sparse previous literature. Because oflimited data availability, the remaining summariesof the pooled data concentrate on the C-G, S-Gand Pr; and only for the metals Zn, Cu, Pb andCd.

3.2. Relationships between organism and sedimentrwater metal concentrations

Each of the relationships between organismand environmental media has shown a character-istic scatter of points within the data. This scattervaries with each individual relationship; i.e. abroad scatter of data for all Cd relationships, anda narrow scatter in the relationships involvingwater Cu levels with animals of any feeding guild.Possible explanations for this are numerous and

Ž .include: i variation in the diet of different speciesŽ .within a feeding guild; ii the metal species in-

Ž .volved in each investigation; iii the geographicalŽ .location the organisms were collected from; iv

Ž .incorrect classification of feeding guilds; v rela-tive ages of the individuals used in each of the

Ž .feeding guilds; vi variations in the preparationand analysis of samples from each investigation;

( )K.L. Goodyear, S. McNeill r The Science of the Total En¨ironment 229 1999 1]19 5

Ž .vii accuracy of the results used, only mean val-ues were used from each reference and no ac-count of concentration ranges was considered;

Ž .and viii variation in water pH, Eh, temperature,hardness, etc., between the investigations. Never-theless, despite their co-variant factors it is obvi-ous that overall general relationships exist linkingmetal concentrations in the environment to thosein the animals.

3.3. Zinc

The pooled data show that relationshipsbetween Zn concentrations in sediments and in

macro-invertebrates are significant for each ofthe feeding guilds C-G, S-G and Pr, at the 1%

2 Žlevel and have high adjusted R -values Fig. 1,.Table 3 . Regression analysis of the relationships

between Zn concentrations in sediments and or-ganisms illustrate that each feeding guild has asignificant slope and intercept value. Zinc levelsin animals appear to be taken up in direct propor-tion to levels in the sediments. Concentrations ofZn in animals increase along the gradient C-G)S-G)Pr, at similar sediment Zn levels.

Relationships between water Zn concentrationsand those in each feeding guild have significant

Ž . 2r-values 1% level , but low R -adjusted values

Table 3Summary statistics describing the relationships between Zn, Cu, Pb and Cd concentrations in sediments and waters with those in

aaquatic macro-invertebrates

2N R Regression equation Intercept R -adjustedŽ .P %

UUZn sediment: Collectorrgatherer 159 0.908 Animal Znsy1413q5.57x -0.001 82.3UUScraperrgrazer 38 0.766 Animal Zns707q0.43 x -0.001 57.6UUPredator 98 0.981 Animal Znsy1139q2.67x -0.001 75.7

UUZn waters: Collectorrgatherer 158 0.231 Animal Zns1222q0.492 x -0.001 4.7UUScraperrgrazer 16 0.713 Animal Zns89.1 x 0.155 47.3UUPredator 90 0.411 Animal Zns555q0.11 x -0.001 16.0

UUCu sediment: Collectorrgatherer 121 0.810 Animal Cus0.294 x 0.285 65.2UUScraperrgrazer 36 0.814 Animal Cus1.73 x 0.298 65.3UUPredator 40 0.946 Animal Cus26.2q0.114 x -0.001 89.2

UUCu waters: Collectorrgatherer 147 0.948 Animal Cus0.904 x 0.244 89.2UUScraperrgrazer 32 0.890 Animal Cus107q0.297x -0.001 78.5UUPredator 61 0.908 Animal Cus87.4q0.209 x 0.008 82.1

UUPb sediment: Collectorrgatherer 148 0.389 Animal Pbs0.109 x 0.085 14.5UUScraperrgrazer 46 0.365 Animal Pbs0.459 x 0.154 11.4UUPredator 99 0.375 Animal Pbs73.3q0.067x 0.036 13.2

UUPb waters: Collectorrgatherer 113 0.973 Animal Pbs11.6 x 0.826 94.6UUScraperrgrazer 20 0.672 Animal Pbsy405q107x 0.024 42.1UUPredator 75 0.979 Animal Pbs99.8q0.401 x -0.001 95.7

UUCd sediment: Collectorrgatherer 168 0.348 Animal Cds7.19q0.364 x -0.001 11.6UUScraperrgrazer 35 0.535 Animal Cds2.17x 0.081 26.4UUPredator 99 0.247 Animal Cds3.16q0.663 x 0.031 5.1

Cd waters: Collectorrgatherer 98 0.071 Animal Cds20.3 -0.001 0.0UUScraperrgrazer 11 0.822 Animal Cds0.971 x 0.290 64.0

Predator 64 y0.011 Animal Cds11.9 0.040 0.0

a These relationships are presented in Figs. 4 and 5, and these should be used in conjunction with this table.

( )K.L. Goodyear, S. McNeill r The Science of the Total En¨ironment 229 1999 1]196

Ž .Fig. 1. Relationships between Zn concentrations in macro-invertebrates of different feeding guilds with those in A sediments orŽ .B waters. Figure should be used in conjunction with Table 3.

Ž .C-G, 4.7%; S-G, 47.3%; and Pr, 16%; Table 3 .Concentrations of Zn in the animals appear to bemore or less regulated regardless of concentra-tions in the waters; regression equations con-firming these relationships. It appears that Znconcentrations in C-G are higher than in Pr atlower water Zn concentrations, but are lowerthan Pr at higher water Zn concentrationsŽ .Fig. 1 . Significant positive relationships betweenZn concentrations in waters and in insect larvaehave been documented previously, e.g. VuoriŽ .1993 found relationships for Hydropsyche an-

Ž . Ž .gustipennis and H. pellucidula Trichoptera C-G ,Ž .and Timmermans et al. 1992 for Mystacides sp.

Ž . Ž .Trichoptera C-G . Therefore when consideringZn bioaccumulation in aquatic macro-in-

vertebrates it is important to know whether theZn is in a particulate or soluble phase, and towhich feeding guild the animal belongs. Further-more, Zn biomagnification does not seem to beoccurring between these groups of animals, as Znconcentrations in animals taken from similar en-vironmental concentrations do not significantlyincrease in animals of a higher trophic level.

3.4. Copper

Each of the feeding guilds of macro-in-vertebrate, C-G, S-G and Pr, have body Cu con-centrations in similar relationships with sediment

Ž .Cu concentrations Fig. 2 , whereby body concen-trations increase as sediment concentrations in-

( )K.L. Goodyear, S. McNeill r The Science of the Total En¨ironment 229 1999 1]19 7

Ž .Fig. 2. Relationships between Cu concentrations in macro-invertebrates of different feeding guilds with those in A sediments orŽ .B waters. Figure should be used in conjunction with Table 3.

crease. Significant r-values and high R2-adjustedvalues for each relationship confirm the visually-obvious relationships. Regression analyses of therelationships give significant slope and intercept

Ž .values Table 3 . Copper concentrations in thethese feeding guilds follow the gradient S-G)C-G)Pr.

Significant relationships between animal Cuconcentrations and those in water are highlightedby the r-values, high R2-adjusted values and thesignificant slope and intercept values for each

Ž .regression equation Fig. 2, Table 3 . It is notpossible to determine a Cu concentration gradi-ent between the feeding guilds as the cloud ofpoints for each guild overlaps with the others.

Ž .Previously, Nehring 1976 illustrated thatŽ . Ž .Ephemerella grandis Ephemeroptera C-G andŽ . Ž .Pteronarcys californica Plecoptera Pr accumu-

lated Cu in proportion to concentrations in wa-ters. It appears that macro-invertebrates bioaccu-mulate Cu, and that they do so from both particu-late and soluble sources. Because there is nosignificant difference in the intercept valuesbetween guilds, there appears to be no biomagni-fication of Cu.

3.5. Lead

The relationships between Pb concentrations insediments and in C-G and Pr feeding guilds of

( )K.L. Goodyear, S. McNeill r The Science of the Total En¨ironment 229 1999 1]198

macro-invertebrates are significant at the 1%level. These two feeding guilds have significantregression lines and intercept values, but low

2 Ž .R -adjusted values Fig. 3, Table 3 . Conversely,the relationship involving S-G animals is not sig-nificant and does not have a significant interceptvalue. This suggests that the S-G is interacting ina different manner with sediments than the C-Gor Pr guilds. No Pb concentration gradientbetween the feeding guilds can be established, asdata for all guilds fall within one cloud of points.

Ž .Eyres and Pugh-Thomas 1978 and TimmermansŽ .et al. 1989 both found that Pb concentrations

were lower in carnivorous species than those ofother guilds, but the data here suggest the oppo-

site, with the Pr guild having greater amountsthan the S-G.

All relationships between Pb concentrations inmacro-invertebrates and in waters are significantŽ .Table 3 . The guilds S-G and Pr have both sig-nificant slopes and intercepts, while the C-G only

Ž .has a significant slope Fig. 3 . A broad concen-tration gradient between the guilds is suggestedto be C-GsS-G-Pr. Positive significant rela-tionships between Pb concentrations in waters

Ž .and in Ephemerella grandis EphemeropteraŽ . Ž .C-G , Pteronarcys californica PlecopteraŽ . Ž .Pr Nehring 1976 , Hexagenia limbataŽ . Ž . Ž .Ephemeroptera C-G Besser and Rabeni 1987

Ž . Ž .and Ecdyonurus ¨enosus Ephemeroptera C-G

Ž .Fig. 3. Relationships between Pb concentrationd in macro-invertebrates of different feeding guilds with those in A sediments orŽ .B waters. Figure should be used in conjunction with Table 3.

( )K.L. Goodyear, S. McNeill r The Science of the Total En¨ironment 229 1999 1]19 9

Ž .Burrows and Whitton 1983 have previously beendocumented. The individual feeding guilds ofmacro-invertebrates are therefore not interactingsimilarly with Pb in the particulate and solublephases, and Pb biomagnification may be occur-ring.

3.6. Cadmium

Relationships involving Cd concentrations inthe sediments and waters are more difficult tointerpret, as concentrations are always low, near-ing the detection limit of the instrumentation onwhich they were made. For this reason, the sum-mary offered below is at best a suggestion ofpossible relationships between the media.

Only the feeding guilds C-G and S-G havepossible relationships with sediment Cd concen-trations. Furthermore, the C-G are the only guild

Žto have a significant regression equation Table.3 . All guilds have data which plot within one

widely-scattered cloud. Relationships involvingwater and animal Cd concentrations fail to pro-duce any significant relationships. This is probablythe result of poor data precision.

Many authors have suggested there are goodrelationships between Cd and Zn concentrationsin waters and organisms, and that relationshipsinvolving Zn may be used as tracers for Cd rela-

Ž .tionships, e.g. Clubb et al. 1975a,b , Carter andŽ . Ž .Nicholas 1978 , Dressing et al. 1982 , Burrows

Ž . Ž .and Whitton 1983 , Memmert 1987 and BarakŽ .and Mason 1989 . This may be so but the present

data for Cd are too poor to show whether this isgenerally the case or not.

3.7. Relationships between concentrations of differenthea¨y metals within feeding guilds

3.7.1. Collector]gathererFig. 4a and Fig. 5a illustrate relationships

between heavy metal concentrations in organismsof the C-G feeding guild and sediments or waters,respectively. Levels of Zn, Cu, Pb, Cd in organ-isms are found in direct proportion to those insediments, suggesting that the organisms metalconcentrations are heavily influenced by the sedi-

Ž .ment metal levels Fig. 4a . The same relationship

is found between organism and water metal con-centrations, although water metal concentrations

Žare very much less than those in organisms Fig..5a . The concentration gradient between metal

levels in organisms and sediments or waters is thesame, Cd-Pb FCu F Zn. In turn this suggeststhat the sediment and water metal concentrationsare in close association, and that the organismsare interacting with both sources of the metals, asmight be expected with animals that burrowthrough the sediment. Significant relationshipsbetween metal levels in sediments and C-G were

Ž . wfound by Jop 1991 Ephemera danica andŽ .xE. ¨ulgata Ephemeroptera and Hare et al.

Ž . w Ž .x1991a,b Hexagenia rigida Ephemeroptera .

3.7.2. Scraper]grazersFig. 4b and Fig. 5b illustrate relationships

between metal concentrations in organisms of theS-G feeding guild and sediments or waters, re-spectively. In both relationships data points arefew in number. It would appear that concentra-tions of Zn, Cu and Cd in sediments and organ-isms are equable, but that Pb concentrations in

Ž .organisms are less than sediments Fig. 4b . Therelationship between metal concentrations in S-Gand sediments follows a simple gradient: Cd-PbsCusZn. No further explanation of this rela-tionship may be made with the available data.Too few data are available to assess concentra-tion gradients of heavy metals in organisms with

Ž .relation to water concentrations Fig. 5b . It maybe that Cu is accumulated to low levels by theS-G, but more data are needed to verify thisrelationship.

3.7.3. PredatorFig. 4c and Fig. 5c illustrate relationships

between metal concentrations in organisms of thePr feeding guild and sediments or waters, respec-tively. The Pr appear to accumulate Cd and Zn indirect proportion to those levels in the sediments,with Zn)Cd. Copper and Pb are also accumu-lated by the organisms, but at levels below thosefound in sediments. Only a very generalised con-centration gradient of metal concentrations in thePr can be made, and that is Cd-PbsCusZnŽ .Fig. 4c , following that for the S-G. Linear rela-

( )K.L. Goodyear, S. McNeill r The Science of the Total En¨ironment 229 1999 1]1910

Fig. 4. Relationships between Zn, Cu, Pb and Cd concentrations in sediments with those in macro-invertebrates of different feedingguilds. Attention is drawn to the unequal distribution of data between the guilds, and the differences in concentrations of eachmetal in the individual guilds.

( )K.L. Goodyear, S. McNeill r The Science of the Total En¨ironment 229 1999 1]19 11

Fig. 5. Relationships between Zn, Cu, Pb and Cd concentrations in waters with those in macro-invertebrates of different feedingguilds. Attention is drawn to the unequal distribution of data between the guilds, and the differences in concentrations of eachmetal in the individual guilds.

( )K.L. Goodyear, S. McNeill r The Science of the Total En¨ironment 229 1999 1]1912

tionships between Zn and Cu concentrations inwaters and Pr are found, with Zn being regulatedat approximately 1000 mgrg and Cu being accu-mulated to levels equal to those found in sedi-

Ž .ments Fig. 5c . There are no clear relationshipsbetween levels of Pb and Cd in animals andwaters, probably because the low concentrationsof metals found in the Pr, and often waters, arehard to determine with any accuracy. Data for Pband Cd appear to cluster and little interpretationabout their bioaccumulation can be made fromthe available literature. A generalised concentra-tion gradient of metal concentrations in predatorsfollows thus: Cd-Pb-CuFZn.

4. Discussion and conclusion

Statistical analyses of the relationships betweenZn concentrations in macro-invertebrates andsediments or waters suggests that they are sig-nificant. There appear to be no differences in therelationships between the feeding guilds. Thegraphical representation of the data shows thereis regulation or restriction of Zn uptake from theaqueous sources. The relationship involving sedi-ments on the other hand, suggests that the ani-mals accumulate Zn in direct proportion to sedi-ment levels. The source of Zn, either aqueous orparticulate, is therefore an important aspect ofthe concentrations found in macro-invertebrates.

Copper and Pb concentrations in organisms ofeach feeding guild significantly correlate withthose in sediments and waters. Concentrations inanimals are always more than in waters, but areusually less than in sediments, irrespective offeeding type. Levels of Cu and Pb in the environ-ment appear therefore to greatly affect thewhole-animal metal concentrations, as Cu and Pbconcentrations increase in proportion to those inthe environment with no signs of biological limi-tation. Biomagnification of Cu does not seem tobe occurring between guilds as the levels of thismetal do not appear to be higher at higher trophiclevels. Biomagnification of Pb may occur, as con-centrations in Pr are often significantly higherthan S-G at many environmental concentrations.

Relationships between Cd concentrations in in-

sect larvae and waters or sediments are hard tointerpret, as many Cd concentrations are close tothe detection limit of the instrumentation used.There appear to be no significant relationshipsbetween water and animal Cd concentrations, butthere are significant relationships between sedi-ment and animal Cd concentrations. These latterrelationships do not produce convincing bivariateplots.

Biomagnification is a phenomenon which is todate not fully understood. It is imperative tounderstand biomagnification if the protection oforganisms of all trophic levels is to be considered.An understanding of the metal content of foodsources of higher trophic levels, and the environ-ment in which they live, must be assessedŽ .Timmermans et al., 1992 . Several previous in-

Ž .vestigations, e.g. Memmert 1987 and ProsiŽ .1989 , have shown that biomagnification of Pband Cd do not take place, but Timmermans et al.Ž .1989 suggested that Zn biomagnification didoccur, in their investigation of food-web chem-istry. The work presented above would suggestthat Zn and Cu are not biomagnified by freshwa-ter macro-invertebrates, Pb may be in some cir-cumstances, and it is impossible to determine ifCd is biomagnified with this dataset.

To date, there is a lack of available data aboutmetal bioaccumulation by freshwater macro-in-vertebrates. As a result, relationships betweenenvironmental metal concentrations and those in

Ž .organisms are not well understood. Kelly 1988notes that the small number of organisms used inmany relationships between metal concentrationsin waters and organisms may account for therelatively few significant correlations found. Hesuggests that ‘more extensive sampling of particu-lar groups may reveal better correlations’. Thepurpose of this investigation has been to increasethe number of data points available and to try toestablish clearer general relationships betweenmetal levels in various groups of macro-in-vertebrates and environmental media. Further in-vestigations of more species, for more metals, andover greater concentration ranges are needed todevelop the understanding of bioaccumulationand biomagnification in freshwater macro-in-vertebrates.

( )K.L. Goodyear, S. McNeill r The Science of the Total En¨ironment 229 1999 1]19 13

Acknowledgements

The European Social Fund is thanked for sup-plying the funding to undertake this work as part

Ž .of PhD research K.L. Goodyear . The GeologyDepartment at Imperial College, University ofLondon, is also thanked for further financial help,and use of their equipment, during the research.

Appendix A

Summary of the available literature on heavymetal bioaccumulation by aquatic macro-in-vertebrates. Attention should be paid to the vari-ety of species used and the lack of studies investi-gating the same species. Full references are givenin the reference list.

Macro-invertebrate Authors Other Environ- FeedingMetalsment. guildCd Pb Cu Zn

ARTHROPODA

CRUSTACEA

MALACOSTRACA

Ž .Amphipoda sandhoppers

Gammaridae Zauke, 1982 r Stream ShGammarus pulex Jop and Wojtan, 1982 r r Stream ShGammarus pulex Khan, 1995 r Lab. ShGammarus pulex Xu and Pascoe, 1994 r Lab. ShGammarus pseudolimnaeus Spehar et al., 1978 r r Lab. ShGammarus sp. Barak and Mason, 1989 r r Hg Stream Sh

Ž .Isopoda woodliceAsellidae

Asellus aquaticus Jop and Wojtan, 1982 r r Stream ShrGrAsellus aquaticus Eyres and Pugh-Thomas, r r r Stream ShrGr

1978Asellus aquaticus van Hattum et al., 1989 r Lab. ShrGrAsellus meridianus Rac Brown, 1977b r r Lab. ShrGrAsellus communis Lewis and McIntosh, 1986 r r Lab. ShrGrAsellus sp. Anderson et al., 1978 r r r r Stream ShrGr

Asellus sp. Dixit and Witcomb, 1983 r r r Stream ShrGrAsellus sp. Barak and Mason, 1989 r r Hg Stream ShrGr

Ž .Decapoda crayfishAstacidae.

Orconectes sp. Anderson et al., 1978 r r r r Stream Fi

( )UNIRAMIA insectsPTERYGOTA

Ž .Ephemeroptera mayflies Barak and Mason, 1989 r r Hg StreamEphemeridae

Hexagenia bilineata Dukerschein et al., 1992 r Hg Stream C-GHexagenia limbata Hare et al., 1989 r r r As Stream C-GHexagenia limbata Hare and Campbell, 1992 r r r Lake C-GHexagenia limbata Besser and Rabeni, 1987 r Lab. C-GHexagenia rigida Hare et al., 1991b r r r Lake C-GHexagenia sp. Anderson et al., 1978 r r r r Stream C-GHexagenia sp. Beauvais et al., 1995 r Hg Stream C-GHexagenia sp. Anderson, 1977 r r r r Stream C-GEphemera danica Jop, 1991 r r r r Stream C-G

( )K.L. Goodyear, S. McNeill r The Science of the Total En¨ironment 229 1999 1]1914

Ž .Continued

Macro-invertebrate Authors Other Environ- FeedingMetalsment. guildCd Pb Cu Zn

Ephemera danica Jop and Wojtan, 1982 r r Stream C-GEphemera danica Goodyear, 1997 r r r Fe, Mn Stream C-GEphemera ¨ulgata Jop, 1991 r r r r Stream C-G

PotamanthidaePotamanthus sp. Anderson, 1977 r r r r Stream C-G

EcdyonuridaeEcdyonurus ¨enosus Burrows and Whitton, 1983 r r r StreamEcdyonurus ¨enosus Goodyear, 1997 r r r r Fe, Mn StreamStenonema modestum Smock, 1983 Co, Cr, Fe, Lab. C-G

Mn, Sb, ScStenacron interpunctatum Smock, 1983 Co, Cr, Fe Lab. C-G

Mn, Sb, ScStenonema sp. Anderson, 1977 r r r r Stream C-GRithrogena sp. Burrows and Whitton, 1983 r r r Stream C-G

EphemerellidaeDrunella doddsi Colborn, 1982 Mo Stream C-GDrunella grandis Colborn, 1982 Mo Stream C-GEphemerella ignita Burrows and Whitton, 1983 r r r Stream C-GEphemerella grandis Nehring, 1976 r r r Ag Lab. C-GEphemerella grandis Clubb et al., 1975a r Lab. C-GEphemerella grandis Clubb et al., 1975b r Lab. C-G

LeptophlebidaeLeptophlebia ¨espertina Jop, 1991 r r r r Stream C-G

Baetidae Saiki et al., 1995 r r r Stream C-GBaetis rhodani Rehfeldt and Sochtig, 1991 r r r r Stream C-G¨Baetis ¨ernus Jop, 1991 r r r r Stream C-GBaetis sp. Kiffney and Clements, 1993 r r r Stream C-GBaetis sp. Anderson, 1977 r r r r Stream C-G

Baetis sp. Burrows and Whitton, 1983 r r r Stream C-G

Ž .Odonata dragonflies Brown, 1977a r r Fe Stream PrAeshnidae

Anax sp. Anderson, 1977 r r r r Stream Pr

Agriidae Barak and Mason, 1989 r r Hg Stream PrArgia sp. Anderson, 1977 r r r r Stream PrAmphiagrion sp. Anderson, 1977 r r r r Stream Pr

Ž .Plecoptera stoneflies Brown, 1977a r r Fe StreamTaenopterygidae

Brachyptera risi Burrows and Whitton, 1983 r r r Stream Pr

NemouridaeAmphinemura sulcicollis Burrows and Whitton, 1983 r r r Stream Pr

LeuctridaeLeuctra sp. Burrows and Whitton, 1983 r r r Stream Pr

( )K.L. Goodyear, S. McNeill r The Science of the Total En¨ironment 229 1999 1]19 15

Ž .Continued

Macro-invertebrate Authors Other Environ- FeedingMetalsment. guildCd Pb Cu Zn

PerlidaeClassenia sabulosa Cain et al., 1992 r r r r Stream PrClassenia sabulosa Moore et al., 1991 r r r As, Ni Stream PrHesperoperla pacifica Cain et al., 1992 r r r r Stream PrHesperoperla pacifica Moore et al., 1991 r r r As, Ni Stream PrPerla bipunctata Burrows and Whitton, 1983 r r r Stream Pr

PteronarcidaePteronarcys californica Cain et al., 1992 r r r r Stream PrPteronarcys californica Nehring, 1976 r r r Ag Lab. PrPteronarcys californica Clubb et al., 1975b r Lab. PrPteronarcys dorsata Spehar et al., 1978 r r Lab. PrPteronarcella badia Kiffney and Clements, 1993 r r r Stream PrPteronarcella badia Clubb et al., 1975a r Lab. PrPteronarcella badia Clubb et al., 1975b r Lab. PrAcroneuria pacifica Clubb et al., 1975a r Lab. Pr

PerlodidaeMegarcys signata Colborn, 1982 Mo Stream PrSkwala americana Kiffney and Clements, 1993 r r r Stream PrIsoperla grammatica Burrows and Whitton, 1983 r r r Stream PrIsoperla grammatica Goodyear, 1997 r r r r Fe, Mn Stream PrPerloides microcephala Burrows and Whitton, 1983 r r r Stream PrArcynopteryx signata Clubb et al., 1975b r Lab. PrIsogenoides sp. Cain et al., 1992 r r r r Stream Pr

ChloroperlidaeChloroperla sp. Burrows and Whitton, 1983 r r r Stream Pr

Ž .Hemiptera bugsCorixidae

Sigara sp. Barak and Mason, 1989 r r Hg Stream PrSigara sp. Anderson et al., 1978 r r r r Stream Pr

Ž .Megaloptera alderfliesSialidae

Sialis sp. Hare and Campbell, 1992 r r r Lake PrSialis sp. Barak and Mason, 1989 r r Hg Stream PrSialis sp. Hare et al., 1991a r r r r As Lake Pr

Ž .Neuroptera lacewings Brown, 1977a r r Fe Stream

Ž .Trichoptera caddisfliesRhyacophilidae

Rhyacophilla nubila Vuori, 1993 r r r r Al, Fe Stream PrRhyacophilla dorsalis Burrows and Whitton, 1983 r r r Stream PrRhyacophilla sp. Kiffney and Clements, 1993 r r r Stream Pr

PolycentropidaePolycentropus Burrows and Whitton, 1983 r r r Stream Prfla¨omaculatus

HydropsychidaePlectrocnemia conspersa Darlington et al., 1987 r Stream PrPlectrocnemia conspersa Gower and Darlington, 1990 r Stream Pr

( )K.L. Goodyear, S. McNeill r The Science of the Total En¨ironment 229 1999 1]1916

Ž .Continued

Macro-invertebrate Authors Other Environ- FeedingMetalsment. guildCd Pb Cu Zn

Arctopsyche grandis Cain et al., 1992 r r r r Stream C-GArctopsyche grandis Moore et al., 1991 r r r As, Ni Stream C-GArctopsyche grandis Kiffney and Clements, 1993 r r r Stream C-GHydropsyche pellucidula Vuori, 1993 r r r r Al, Fe Stream C-GHydropsyche pellucidula Burrows and Whitton, 1983 r r r Stream C-GHydropsyche angustipennis Vuori, 1993 r r r r Al, Fe Stream C-GHydropsyche angustipennis Khan, 1995 r Lab. C-GHydropsyche siltalai Goodyear, 1997 r r r r Fe, Mn Stream C-GHydropsyche instabilis Goodyear, 1997 r r r Fe, Mn Stream C-GHydropsyche sp. Cain et al., 1992 r r r r Stream C-GHydropsyche sp. Anderson et al., 1978 r r r r Stream C-GHydropsyche sp. Anderson, 1977 r r r r Stream C-GHydropsyche sp. Colborn, 1982 Mo Stream C-G

Hydropsyche sp. Dressing et al., 1982 r Lab. C-G

BracycentridaeBrachycentrus americanus Clubb et al., 1975a r Lab. C-GBrachycentrus americanus Clubb et al., 1975b r Lab. C-GBrachycentrus sp. Moore et al., 1991 r r r As, Ni Stream C-GBrachycentrus sp. Spehar et al., 1978 r r Lab. C-G

PhryganeidaePhryganea sp. Iivonen et al., 1992 r r r r Ni Lake C-GCheumatopsyche sp. Anderson, 1977 r r r r Stream C-GCheumatopsyche sp. Anderson et al., 1978 r r r r Stream C-G

Limnephilidae Burrows and Whitton, r r r Stream C-G1983

Potamophylax latipennis Vuori, 1993 r r r r Al, Fe Stream C-GLimnephilus sp. Iivonen et al., 1992 r r r r Ni Lake C-G

Limnephilus sp. Moore et al., 1991 r r r As, Ni Stream C-G

LeptoceridaeMystacides sp. Timmermans et al., 1992 r r Lab. C-G

Ž .Diptera true fliesNematocera

TipulidaeTipula sp. Burrows and Whitton, 1983Dicranota sp. Clubb et al., 1975b r r r Stream C-GHexatoma sp. Clubb et al., 1975b r Lab. PrHolorusia sp. Burrows and Whitton, 1983 r Lab. Pr

Chaoboridae r r r Stream PrChaoborus punctipennis Hare and Campbell, 1992Chaoborus sp. Groulx and Lasenby, 1992 r r r Lake Pr

Simulidae r Lake PrSimulium sp. Carter and Nicholas, 1978Simulium ornatipes Anderson et al., 1978 r Lab. FiSimulium sp. Burrows and Whitton, 1983 r r r r Stream Fi

( )K.L. Goodyear, S. McNeill r The Science of the Total En¨ironment 229 1999 1]19 17

Ž .Continued

Macro-invertebrate Authors Other Environ- FeedingMetalsment. guildCd Pb Cu Zn

Simulium sp. Anderson, 1977 r r r Stream FiChironomidae Anderson, 1977 r r r r Stream Fi

Saiki et al., 1995 r r r r Streamr r r Stream

Chironomus riparius Besser and Rabeni, 1987 r Lab. C-GChironomus riparius Williams et al., 1986 r Lab. C-GChironomus riparius Timmermans and Walker, r r Lab. C-G

1989Chironomus thummi Seidman et al., 1986 r Lab. C-GChironomus tetans Gauss et al., 1985 r Lab. C-GChironomus tentans Phipps et al., 1995 r r r r Ni Lab. C-GChironomus sp. Anderson et al., 1978 r r r r Stream C-GChironomus sp. Hare and Campbell, 1992 r r r Lake C-GChironomus sp. Hare et al., 1991a r r r r As Lake C-GChironomus sp. Krantzberg and Stokes, 1988 r r r Al, Mn, Ni Stream C-G

Chironomus sp. Burrows and Whitton, 1983 r r r Stream C-GChironomus sp. Krantzberg, 1989 r r Mn, Ni, Fe Lab. C-GChironomus sp. Krantzberg and Stokes, 1989 r r r r Ni, Mn Lab.rlakes C-GChironomids Krantzberg and Stokes, 1989 r r r r Ni Mn Lakesrlab. C-GChironomids Chapman, 1985 r r r Fe, Mn, Stream C-G

Ni, CoChironomids Dixit and Witcomb, 1983 r r r Stream C-GStictochironomus histrio Timmermans and Walker, 1989 r r Lab. C-GGlyptotendipes sp. St. Louis, 1993 r r Al, Fe, Lake C-G

Mg, MnClinotanypus sp. Hare and Campbell, 1992 r r r Lake C-GProcladius sp. Hare et al., 1991a r r r r As Lake PrProcladius sp. Hare and Campbell, 1992 r r r Lake Pr

BrachyceraRhagionidae

Atherix ¨ariegata Clubb et al., 1975b r Lab. Pr

Ž .Coleoptera beetles Hare et al., 1991a r r r r As Lake PrDytiscidae

Dytiscus sp. Barak and Mason, 1989 r r Hg Stream PrOreodytes sanmarki Burrows and Whitton, 1983 r r r Stream Pr

ElminthidaeLimnius ¨olckmari Burrows and Whitton, 1983 rrrrr r r Stream Pr

Sh, shredder; S-G, scraper]grazer; C-G, collector]gatherer; Fi, filterer; Pr, predator.

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