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M. Stephenson1and C. L. Mackie
Department of Zoology, University of Cuelph, Guelph, Ont. N 9 C 2W1
Stephenson, M., and 6 . L. Mackie. 1988. Multivariate analysis of correlations between environmental parameters
and cadmium concentrations in Hyalella azteca (Crustacea: Amphipda) from central Ontario Bakes.
Can. j. Fish. Aquat. Sci. 45: 1705-1 75 0.
Cadmium concentrations in Hyalelda azteca collected from 69 central Ontario Bakes ranged from 8.1 3 to 56.6
kg/$dry mass. Principal components analysis followed by multiple linear regression found three principal components, interpreted as water hardness, total cadmium, and dissolved organic carbon concentrations, to be significantly (p =S 0.002) correlated with cadmium concentrations in H . azteca. Cadmium concentrations in H.
azteca were independent of cadmium concentrations in littoral sediments. It i s suggested that cadmium ions
compete with calcium ions for uptake sites on the gill surfaces of H. azteca. High concentrations of dissolved
organic carbon may complex free cadmium ions and reduce their concentration in solution, leading to lower
cadmium concentrations in H. azteca.
Les teneldrs en cadmium chez des specimens d'Hyalella azteca prelev6s dans 69 Bacs du centre de ItOntario
6taient comprises entre 0,13 et 56,6
de masse sGche. L'analyse des cornposantes principales suivie d'une
regression lineaire multiple a permis de dkceler une correlation significative (p
0,002) entre trois grandes
composantes (durete de I'eau, cadmium total et concentration en carbone organique dissous) et les teneurs en
cadmium relevees chez H. azteca. Les teneurs en cadmium chez H. azteca 6taient independantes de la teneur
en cadmium des sgdiments Iittoraux. Ces donnees semblent indiquer que les ions cadmium rivalisent avec les
ions calcium pour les sites de fixation la surface des branchies chez H. azteca. Des teneurs elevees en carbone
organique dissous peuvent former des complexes avec des ions cadmium libres et r a u i r e Jeur concentration
dans la solution, ce qui entraine des tenem en cadmium plus faibles chez 68. azteca.
R e p le 3 judlet 3987
Accept4 le 3 1 mai 3 988
(J9.344)
Methods
Seventy-five central Ontario lakes (Fig. 1) were sampled
between July 17, 1984, and August 15, 1984, by scraping surface sediments with a stainless-steel sieve (0.32 mm)md examining the sediments ret.eved for H. azteca. Hyalehla azteca!
was found in 69 lakes. Animals were sorted with stainless-steel
forceps into acid-cleaned polypropylene cups filled with clean
lake water. They were kept cool for 24 h to allow gut clearance
and then frozen in distilled-deionized water in acid-cleaned
polypropylene vials. The animals were subsequently thawed,
placed in acid-rinsed polystyrene tissue culture dishes (35 X
10 m),and examined under a dissecting microscope. Undmaged animals with 890 observable gut contents (10 per lake when
possible) were individually placed in acid-cleaned 1.5-mE
poiypropylene microcentrifuge tubes and oven dried (55C)
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FIG. 1 . Central Ontario showing the locations of the study lakes. The square in the inset map sf Canada
shows the approximate location of the study m a .
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Lake
Richard
McFarlane
Raft
hhi
Clearwater
Simn
McCharles
Attlee
Gainey
Broker
Tyson
Mahzenazing
Kakakiwaganda
Township
H m
Dill
BroderIDill
DillIBroder
Broder
Broder
Graham
Grahm
Attlee
Attlw
Attlee
SalelAttlee
Humboldt
Servos
Bigwssd
Sollmm
Cecebe
Ahmic
Old Man's
Bell's (Silver)
Spence
Horn
Bear
Rdney
Bray
King
Eagle
Deer
Lk. M. Islands
Vhalley
Chapman
Chapman
Chapmadcroft
Spence
Spence
Spence
Monteith
Montieth
Ryerson
Machar
Machar
Machar
Lount
hunt
ChapHnan/Croft
cm*
McCoy
Hay
McKenzie
Lit. Boulter
Lk. St. Peter
Whitefish
Rock
Louisa
H w
Cache
Source
Potter
Brule
kck
Sabine
Sabine
SabineILyell
McClure
McClure
Sprsule
Nightingale
Lawrence
Lawrence
Canisbay
Peck
PwWHunter
Hunter
Hunter
C ~ P
Lucky
Ohlmmn
Reid
Big Bhlmann
Ban's
Fortune
tong Schooner
Kitchen
Mackie
Shaw
Bmle
endstone
Will's
Buckshot
Miller
Miller
Miller
Miller
Miller
Miller
Miller
Miller
Miller
Miller
Miller
Miller
Miller
CBarendon
Miller
.Toe
TABLE1. (Csnckerded)
Cd in Pi. azteca
Lake
Echo
Ril
Chub
Little Wren
Beech
Maple
Green
Pine
Cranberry
Hv
Lake of Bays
Heeney
Dickie
Plastic
Blue Chalk
Red Chalk
( ~ Cd/g
g dry mass)
Township
Mckan
Ridout
Ridout
Sherbome
Stanhope
Stmhope
Guilfo1.8
Guilford
Guilfsrd
Cbffey
Franklin
Mckm
McLaan
S herbome
Ridout
Ridout
The adequacy of the interpretations of the principal compnents was tested by multiple linear regression using the v k ables loading on the principal components as independent vmiables against Cd concentrations in H. cmztecce. Four sets of
independent variables were tested (Ca2 ,Cd, DOC; ANC, Cd,
DOC; pH, Cd, DOC; Mg2+,Cd, DOC). The model including
Ca2-, Cd, and DOC has the best fit as measured by the a-square,
and the regression is summapized in 'Table 5.
+
Cadmium concentrations in freshwater crustaceans are typically less than 1.0 pg/g dry mass (Zauke I982b; Jop and
Wojtan 1982; Pfosi 1983). Concentrations in excess of 2 pg/g
are generally associated with industrial contamination (Anderson et al. 1978; Kneip and Hazen 1979; Zauke 1981; Jop and
Wo~tan1982;Ddlinger and Kautzky 1985j. Excluding the value
of 56.5 pg/g dry mass obtained for a single specimen from
Plastic Lake, Cd concentrations in H . ceztecce from central
Ontario lakes ranged from 0.13 to 3'9.3 pg/g dry mass. Both
the highest (Heeney Lake) and the lowest (Ohlmmn Lake) concentrations were recorded in remote lakes without known direct
sources of contamination.
Multiple linear regression of Cd concentrations in H . azteca
with the orthogonal-derived vaiiables (principal components)
showed that at least Qkree components account for significant
amounts of variation. Two principd components (PC%,PC3)
have unambiguous interpretations (DOC and total Cd concentrations, respectively). However, PC 1 was strongly correlated
with Ca2 , Mg2+,pH, and ANC. Its interpretation is ambiguous and must focus on whether hardness cations or ANC
(HC0,-, C0,2-) modify the availability of Cd to H . aztecce.
Interactions between water hardness and trace metal toxicity
are well documented. It is thought that the protection afforded
by hardness is due to competition between divalent base (Ca2+,
Mg2+)and trace metal cations for binding sites, thereby reducing uptake and toxicity, Cadmium toxicity to G w m m s pulex
is reduced by high Ca concentrations (Wright and hain 198I),
and the process of Cd accumulation has been linked with Ca
metabolism (Wright 198Q).At "low" Cd concentrations (56 560 pg/L), arn equimolmrelationship between @aand Cd uptake
was implied by Wright (1980). This conclusion is partly SUPported by data from the present study. Although Cd concentra+
TABLE2. Variables included in the full K A matrix, their geometric means, and ranges.
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Variable
Mean
Rmge
ANC (mqlL)
Total P (pglL)
Ca b @ L )
Mg (mgW
Na (mg/L)
K (mg/L)
F oJ&L)
C1 (mg/L)
so4 (mdL)
Total Fe (m@L)
Total Mn (mg/L)
DOC (mg/L)
PH
PC 1
PC2
PC3
0.965
0.902
0.882
0.874
- 0.087
-0.312
0.054
-0.048
0.220
8.122
-0.994
0.055
- 0.179
- 0.352
- 0.360
56.51
-0.114
- 0.043
0.948
17.65
19.98
Variable
SE
0.264
0.148
0.101
0.241
4.47
-7.78
6.36
-3.35
C0.001
<0.001
<8.001
-0.002
Coefficient
Intercept
Ca
@d
DOC
1.182
- 1.154
0.643
- 0.805
r = 0.901
r2 = 0.813
-
- -
Analysis of variance
Source
Regression
df
Sum square
Mean square
15.801
3.645
5.267
0-078
67.92
<0.001
47
Coefficient
Intercept
PC1
K 2
PC3
0.580
- 0.424
0.132
0.342
BP
SE
0.039
0.040
0.040
0.040
14.70
<0.001
<0.001
0.002
C8.001
- 10.64
3.31
8.60
r = 8.898
r2 = 0.808
Analysis of variance
Source
df
Sum square
Mean square
Regression
Residual
3
47
15.717
3,728
5.239
0.079
66.04
<0.001
and excretion. The lower value indicates that some discrimination, either during uptake (i.e. by the cation pump at the gill
surface) or via depuration (selective Cd Boss during excretion,
d y s i s , or other mechmism), may occur.
The second interpretation of PCB (a gradient of increasing
pH and AN@)is the expectation of an interaction between Cd
and bicxbonslbe/cxbonate species which could effectively
complex Cd a d reduce the available cationic fraction of the
total Cd concentration. Gardiner (1974) explored Cd speciation
with a variety of inorganic and organic ligands, using a Cdspecific electrode. He concluded that there was strong evidence
for a soluble Cd.+x.rbonate complex. However, this complex is
weak and only %omsat pH > 8.0. Under conditions typical of
central Ontario lakes, it is unlikely that Cd4xbonate complex
fornation could significantly modify the Cd bioavailability.
High concentrations of DOC reduce Cd concentrations in
H. azteca. The effect of DOC on trace metal bbiavailability is
due to the cheldion or complexation of trace metal ions, largely
onto hnrmic and fnrlvic acids (Neubecker and Allen 1983). Eaboratory studies (Poldoski 1979; Geisy et id. 1977; Dressing et
al. 1982; Winner 1984; Oakden et al. 1984) show that various
size fractions of natural dissolved organic matter, or synthetic
Can. J. Fish. Aquat. Sei., Val. 45, I988
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chelators, may increase or decrease the bioavailability or toxicity of Cd to invertebrates. The net effect of high DOC concentrations in central Ontario lakes is to decrease the availability of Cd to H . azteca, although PC2 (interpreted as DOC)
is much less important as a predictor of Cd concentrations in
H.azteca than PC1 (Ca2+,h4g2+,ANC, pH) and PC3 (total
Cd).
Conclusion
Cadmium concentrations in 8%. azteca are correlated with
water chemistry md are independent of sediment Cd concentrations and basin monphometry. Thee chemical parameters
(Ca2+,total Cd, DOC) explain 8 B -3% of the total variation in
Cd concentrations of H. azteca. It is likely that Ca2+and Cd
compete for uptake, while DOC may complex a portion of the
total aqueous Cd, reducing the available ionic Cd concentration.
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