Metal concentrations of resident and transplanted freshwater mussels Hyridella menziesi (Unionacea: Hyriidae) and sediments in the Waikato River, New Zealand

the Science of the Total Environment

ELSEVIER

The Science of the Total Environment 175 (1995) 163-177

Metal concentrations of resident and transplanted freshwater mussels Hyridella menziesi (Unionacea: Hyriidae) and sediments in the Waikato River, New Zealand C.W. Hickey”, D.S. Ropera, S.J. Bucklandb aNIWA

Ecosystems,

National Institute of Water and Atmospheric bE.SR: EnLironmental, PO Box 30-547,

Research, PO Box 11-115, Lower Hutt, New Zealand

Hamilton,

New Zealand

Received 23 September 1994; accepted 18 January 1995

Abstract Heavy metals and metalloidswere measuredin freshwater mussels (Hyridella menziesi) and sedimentsin the upper Waikato River, New Zealand. Mercury (Hg) concentrationsranged35fold in sediments(0.025-0.87 mg kg-’ dry wt) and 144-fold in mussels(0.091-13.1 mg kg-’ dry wt). Arsenic (As) concentrations ranged 190-fold in sediments (7.9-1520 mg kg-’ dry wt) and only lo-fold in mussels(15.0-153 mg kg-’ dry wt). There was no significant correlation between sedimenttotal concentrationsof either Hg or As and musseltissue levels. Sediment quality guidelineswere exceededfor Hg and As at mostsitesand for copper, chromium, iron and manganeseat a few sites. Tissueconcentrationsexceededlevelsconsideredto be safefor humanconsumptionfor Hg at Lake Aratiatia and As at severalsites.Transplant experimentswith cagedmusselswere usedto measureuptake and depuration ratesof Hg and As. Half-lives for musseluptake and depuration of Hg were 6-12 months. Arsenic uptake rates could not be determinedbut the depuration showeda half-life of about 2.5 months. Physiologicalmeasurementswere consistent with increasedfood availability at somesites rather than contaminant effects. These results highlight the need to understand biochemical changes induced by factors that are independent of environmental concentrations of contaminants, such as the influence of food levels and the potential for metabolic adaptation in biomonitoring organisms. Keywords:

Metals; Mercury; Arsenic; Sediment;Condition; Monitoring; Unionacea

1. Introduction

Determining of contaminant

the presence, extent and degree impact in aquatic ecosystems is a

difficult task. The presence of diffuse agricultural input, multiple municipal or industrial discharges, with changing or intermittent flows, can result in highly variable and complex contaminant mixes.

0048-9697/95/$09.50 0 1995 Elsevier Science BV. All rights reserved. SSDI 0048-9697(95)04722-D

I h4

C: W. Hickey

et al. / The Science

of the Total EnL:ironment

Of the wide variety of organisms which can be used for biomonitoring, shellfish are favoured as they meet the general requirements of biomonitars (Phillips and Rainbow, 19921, and in particular because of their often widespread distribution, ecological importance, sedentary nature, relatively high tolerance to pollutants, bioaccumulation of chemicals, and ability to be transplanted and held in cages (Farrington et al., 1987). Recent reviews have covered the use of mussels as biological indicators of pollution (Viarengo and Canesi, 1991), and freshwater molluscs as indicators of bioavailability and toxicity of metals (Elder and Collins, 1991). The general acceptance of the advantages inherent in the use of shellfish biomonitors has given rise to the establishment of several large monitoring networks (Martin and Severeid, 1984; O’Connor, 1992) and an international shellfish monitoring programme is proposed (Goldberg, 1991). The design of such programmes has been reviewed by Phillips and Segar (1986). They found three common general objectives for such monitoring: (i) the delineation of spatial variations in pollutant abundance and bioavailability; (ii> the elucidation of changes in contaminant bio-availability with time at one or more sites or areas; and (iii> the identification of previously unknown or new contaminants in any given water mass. The Waikato River is New Zealand’s longest and most heavily utilised river. Originating at Lake Taupo on the central North Island volcanic plateau, it runs 327 km northward to discharge into the Tasman Sea with a mean flow of 400 m3 s - ‘. It is the source for over 30 communal drinking water supplies and 200 irrigation withdrawals. It receives 20 major industrial discharges (including a large pulp and paper mill) and several sewage treatment plant discharges, as well as diffuse inputs from numerous geothermal fields, forestry and agricultural activity within the 14300 km2 catchment. It has eight hydroelectric dams and power stations and provides cooling water for two thermal and two geothermal power stations. Natural geothermal areas and geothermal power developments result in elevated concentrations of potentially totic heavy metals (e.g., mercury) and metalloids (e.g., arsenic) (Weissberg and Rohde,

175 (1995)

163-I

7.7

1978; Timperley, 1979). All of these elements may exert direct toxic effects on aquatic biota and may bioaccumulate in organisms consumed by man. Roper and Hickey (1994) have found the New Zealand freshwater mussel HjvideZZu memiesi throughout the Waikato River system. In the Australasian region, populations of freshwater mussels are widespread over large geographic areas (Walker, 1981). Studies with Australian freshwater mussels have indicated that they are suitable for studying bioaccumulation of metals and organic pesticide contaminants (Ryan et al., 1972; Millington and Walker, 1983; Jeffree and Simpson, 1986). Elevated concentrations of sediment arsenic (Aggett and Aspell, 1980; Aggett and Kriegman, 1988) and mercury (Weissberg and Zobel, 1973) are known at some sites, primarily associated with geothermal inputs, though no systematic data is available for the length of the river system. This study was carried out to investigate the nature and extent of chemical contamination of the upper Waikato River using H. menziesi. Metal and metalloid concentrations in sediments were compared to those in resident mussels. Because H. menziesi is a long lived species > 30 years (Roper and Hickey, 1994) accumulated body burdens in resident mussels could reflect historic contaminant levels. To assess present contaminant concentrations transplanted mussels from a common source were caged at the study sites. Physiological measurements were used to assess the level of stress associated with contaminants. 2. Methods

Resident mussels and sediments were sampled in late October 1990, at eight sites along the Waikato River system. These sites included Lake Taupo, the hydro-electric dam lakes of Aratiatia, Ohakuri, Maraetai, Waipapa, Karapiro, and a flowing-water reach at Cobham Bridge, Hamilton (Fig. 1). Additional sampling of mussels and sediments in Aratiatia was performed in December 1991 and of sediment in Waipapa in December 1992 to confirm the mercury (Hg) and arsenic (As) levels found at those sites. Mussels were collected by SCUBA divers and on return to the

C: W. Hickey

et al. / The Science

of the

Total EnL:ironment

I75 (1995)

geothermal, sewage & industrial discharges

0 Sampling sites 1 Hydro-dams ,J!’ Catchment boundary ,<:..

Fig. 1. Location

map for sampling

sites

163-I

77

165

I h(7

C. IK Hickey

et al. / The Science of the Total En;nr;ironment

boat the mussels were placed on ice. At each site five samples of surface sediment (O-5 cm) were collected using a stainless steel scoop from an area of approximately 10 x 10 m and cornposited for particle size and chemical analysis. Table 1 summarises the study site names, locations and abbreviations for sites. Totara Bay was chosen for the Lake Taupo site because James (1985) had shown mussel densities to be particularly high there. This site was used to supply all mussels used in the cage experiments, which were performed in summer/autumn from December 1990 to June 1991. The sites selected for cage locations were below the Wairakei Geothermal Power Station, which contributes 70% of the As and most of the Hg load (Axtmann, 1975; Timperley, 19881, and in Lake Maraetai, which is below most of the smaller inputs from numerous geothermal fields and above the major pulp and paper mill discharge. Cylindrical cages (400 mm long x 150 mm diam.) were constructed of stainless steel mesh (approx. 10 mm aperture). About 100 mussels (40 to 60 mm long) were housed in the three layered cage, which was found to give good survival for 6-12 month deployments. Use of a sub-surface buoy system together with a submerged line to the shore for finding the cages prevented vandalism. The sub-sampling intervals of 1, 3 and 6 months were chosen for transplant experiments based on the likely time for physiological responses and to provide an indication of rate of chemical uptake and depuration. Depuration of Hg from Aratiatia resident mussels and As from Ohakuri resident

I75 (1995)

163-I

77

mussels involved transplantation and caging in Totara Bay, Lake Taupo. Sediments and mussels for Inductively Coupled Plasma (ICP) analysis were freeze-dried prior to analysis. Some mussel samples were subsequently reanalysed by Inductively Coupled Plasma-Mass Spectrometry (ICP-MS), to achieve improved detection limits for cadmium (Cd), nickel (Ni), lead (Pb), cobalt (Co>, chromium (Cr) and selenium (Se). At this time the sediments had been discarded so repeat analyses of the samples could not be undertaken. For each site from the initial 1990 sampling programmes, subsamples from c. 20 mussels were composited to give 2 g dry weight of material. For the sampling in 1991 and the cage experiments composites from 8 mussels were used for analysis. Mussels for ICP analysis were digested with nitric acid, and sediments with nitric acid and hydrofluoric acid prior to analysis. Mussels for ICP-MS analysis were digested with nitric acid and hydrogen peroxide in a microwave procedure. Mercury and As were analysed on homogenised wet samples of 8 mussels and subsamples of dried sediment. A separate portion of mussel homogenate was used for dry weight determination by oven drying at 105°C for 16 h to constant weight. The Hg analysis followed Louie (1983) where a cold nitric/sulphuric/hydrochloric acid digestion was used. Quantitation was by cold vapour generation with stannous chloride reduction. Arsenic determination followed the method of Pickston et al. (1983). The samples were digested with a magnesium nitrate/nitric acid mix-

Table I Site

characteristics

Site

description

(code)

River

distance”

5% Sand

% Silt

% Clay

7% Carbon

(km) Lake

Taupe

Lake Lake

Aratiatia Ohakuri

L.akc Lake Lake

Maraetai Maraetai Waipapa

Lake Karapiro Hamilton (Fi) ‘d~atanw

(Tf

80

1

3.1

I3 69

86 34

2 11

1.4 2.1

1 IO II5 125

42 12 3’ _...

18 20 15

1.9 6.7 15.5

I hi

SO

310

86

78 1

5.1 0.9

-5

(A) (0) (Mu) (Md) (Wt t k:)

II-om

Taupe

Gate.

,327

km L‘rom

Taupe

Gates

to rwer

mouth

C. W. Hickry

et al. /The

Science

of

the Total Enc~ironment

ture and dry ashed at 550°C. Quantitation was by way of hydride generation with sodium borohydride reduction. The Quality Assurance procedure included concurrent analysis of IAEA fish flesh homogenate MA-A-2. A 100% recovery of both As and Hg was achieved. All sediment and mussel tissue results are expressed on a dry wt basis. Mussel tissue dry wt averaged 11% (SD. 1.5%) of the wet wt for homogenised composites of 8 mussels from 6 sites. Physiological measurements included: physical condition, glycogen, protein, filtration and respiration. Mussels from each site were scrubbed clean and rinsed twice in filtered (GFC) river water prior to physiological determinations. Physical condition was determined on 20 mussels and the index calculated as the ratio of flesh dry wt (mg) to shell wt (g). Glycogen content was determined on 10 mussels. The flesh was added to a 50 ml mixture of chloroform/methanol/water (2:4:1; v/v) and homogenised for 1 min with a Sorvall omni-mixer. After centrifugation at 4000 rev./min for 10 min, the centrifugate was removed and the residue extracted with a further 50 ml of solvent mixture. This step was repeated. The residue was then dried at 60°C for 48 h and weighed as the polymeric fraction containing polymeric carbohydrate as glycogen and protein. Glycogen working solutions were prepared by hydrolysing 100 mg of the dried polymeric material with 2 mol 1-r H2S0, at 100°C for 2 h. The hydrolysate was then made up to 50 ml with deionised water and filtered through a Whatman GF/F glass-fibre filter. Subsamples (0.1 ml) of the filtered hydrolysate were analysed for carbohydrate using a phenol-sulphuric acid procedure with D-glucose as the standard. Glycogen values were obtained by multiplying the equivalent glucose values by 0.90. Glycogen content was expressed as % glycogen content of dry wt. Extracts for protein analysis were prepared from the 10 mussels used for glycogen analysis. A 5 mg fraction of the polymeric dried material was analysed for nitrogen using micro-Kjeldahl techniques. Values for nitrogen were multiplied by 6.25 to estimate protein content, which was expressed as % protein content of dry wt. Twelve

I75 (1995)

163-l

77

167

mussels from each site were used for filtration rate measurements (i.e., the rate at which particles are removed from suspension). They were placed individually in glass crystallising dishes containing 100 ml of filtered river water at 20°C collected from the site where the mussels were moored. A neutral red dye stock solution was prepared by dissolving 0.05 g of dye in 50 ml of filtered river water. 100 ml of stock solution was added to each container, giving an initial dye concentration of 1 X 10m3 g 1-l. Mixing of the dyed water was achieved by continuous gentle aeration. Dye was added after the mussels had equilibrated for at least one hour, by which time their siphons were protruding and they were obviously pumping. Two ‘control’ mussels were prevented from pumping by holding the valves closed with rubber bands. Subsamples of the dyed water were taken as soon as it was thoroughly mixed (time 01, and after 15 min. Absorbance of these samples was measured spectophotometrically, at a wavelength of 425 nm. The filtration rate was determined as (Coughlan, 1969): Filtration rate = y log, 2

I

where filtration rate is in ml min- ‘, I/ is the volume of dye solution in the container in ml, C,, is the initial dye concentration (i.e., at time 01, C, is the final dye concentration, and t is the time Filtration interval between samples in hours. rates were corrected for decreases in dye concentration observed in the controls. Filtration rate were expressed as volume pumped (ml> per dry flesh wt (g> per min. Between site comparisons were made using analysis of variance (ANOVA) (Sokal and Rohlf, 1981). Log transformation of condition and physiological values was necessary because of heteroscedasticity of variances. Multiple comparison testing used L.S.D. (Least Significant Difference) for comparison of reference and other sites at a 95% significance level. Levene’s test of homongeneity of variance was used for comparison between sites or sampling intervals (Snedecor and Cochran, 1980). Replicated metals analyses of composited mussel samples were compared using

168

C. W. Hickey

et al. / The Science of the Total Eni:ironment

a Mann-Whitney U-test with a 95% significance level. Relationships between variables was investigated using Spearman-Rank correlations (I, >.

3.1. Resident mussels The initial 1990 survey was performed over the entire length of the river study reach to determine the location and extent of contamination. Mussels were found at each of the sediment sampling sites, although the sediment characteristics did vary between sites (Table 1). Sediments were predominantly sand (> 80%) at the two upper lakes with a downstream increase in clay and silt content. Carbon content averaged 4.6% and

12

E

8

,x

6

2if

4

=

2

163-l

77

ranged from 0.9 to 15.5%. The site furthest downstream (HI was rive&e and predominantly sandy with low clay and carbon levels. The sediment and mussel survey results are shown in Table 2, and summarised in Fig. 2 for the geothermal contaminants Hg and As. Major bioaccumulation of Hg and As in resident mussels occurred in Aratiatia and Ohakuri, respectively. Marked differences occurred between the mussel tissue and sediment concentrations, with the highest Hg concentrations in mussels and As maxima in sediments. Mercury concentrations ranged 35-fold in sediments (0.025-0.87 mg kg-’ dry wt) and 144-fold in mussels (0.091-13.1 mg kg-’ dry wt). Arsenic concentrations ranged 190fold in sediments (7.9-1520 mg kg-’ dry wt) and

3. Results and discussion

‘i 2

17.5 (1995)

n Resident mussels

10

0

-7 800 2 a 300 .k -11 200 t 2 2

100

T

A

0

Mu

Md

W

K

H

Fig. 2. Mercuy (A) and arsenic (B) concentrations in sediment and resident mussels in the Waikato River sampled October 1990. Sites arc: Lakes Taupo CT), Aratiatia (A), Ohakuri (0). Marartai (upstream, Mu). Maraetai (downstream. Md). Waipapa (W), Karapirtr (K) and the river at Hamilton (H).

M M

M M M M M M

S

S

S

S

S

S

Taupo Aratiatia

Ohakuri Maraetai (u) Maraetai (d) Waipapa Karapiro Hamilton

Taupo

Aratiatia

Ohakuri

Maraetai (u)

Maraetai (d)

Hamilton

0.31

.

o.74c

0.12

0.47 0.87’

0.025

0.12 13.1 lo.oc 3.9 0.83 0.41 0.28 0.26 0.091

Hga

295 105

Sr

60.1

101

111_

69.4

7.9

244 218 251 164 201 186

267 313

Zn

11.0 5.8 7.0 9.3 8.9 8.8

6.2 12.7

Cu

-

27.1 70

8.59

19.8 66.2 14.3

-

29.1 52.1 13.4

34.3 33.7 6.82

153 220 19.5 239 23.4 184 22.4 148 15.0 158 15.6 106

62.7 23.9

Asa

25000

30700

-

11900

9840

24500 27800 21300 14400 14100 11400

15700 6620

Fe

1010 845 831 592 766 787

979 886

Mg

611

-

13 300 656

9860

-

14200 1050

13300 938

2020 1590 1960 1210 1630 1860

1880 2140

K

183

-

61.8

69.5

2180 5110 4530 3040 3540 2660

4790 1670

Mn

3940

-

3170

3510

2340 1730 1780 1190 1450 1510

1820 2050

Na

413

-

455

456

21900 23300 20700 14 100 17700 15600

22200 17000

P

334

-

1720

1470

7030 5090 5480 5090 5430 5100

7470 7510

s

26900 186W 17500 11600 16700 12200

19700 13600

Ca

_

llOaO4330

-

110805020

109005600

363 48.8 55.9 125 247 229

< <

Al

<

-

<

<

0.34 0.33 0.74 0.47 0.40 0.25

-

<

-

<

<

1.2 0.70 0.61 0.88 0.64 0.67

<

-

<

<

3.6 0.81 0.90 0.89 0.51 1.6

~~ Nib Pbb ~. 0.25 0.98 4.1 0.21 0.95 14 Cdb

15.3

-

<

<

0.73 0.68 0.64 0.57 0.36 0.47

0.35 0.83

Cob

17.4

-

<

<

1.7 1.5 2.6 2.9 2.5 2.3

2.3 2.2

Crb

<

-

<

<

5.8 2.8 2.7 2.5 2.7 1.9

3.3 9.6

Seb

-

.7*

.-

-

-

--

. I

_

-

-

I

L-I

a

Abbreviations: M = mussels; S = sediment; < = less than detection; - = not determined. Sediment quality guidelines (Persaud, et al. 1992): Box = exceedance of ‘Lowest Effect Level’; Shaded box = exceedance of ‘Severe Effect Level All concentrations in mg/kg dry weight sampled Ott 1990; except ’ = sampled Dee 1991; d = Dee 1992 (ICP analysis) MO, Si and Sn were analysed by ICP but were less than the detection limits. Detection limits (mg kg-‘): ICP - MO = 3.3; Ni = 5.5; Pb = 32; Se = 47.0; Sn = 5.4; Cd = 7.5; Cr = 6.5; As = 61; Si = 3.5; Al = 23 ICP-MS fb) - Cd, Co, Cr, Cu, Ni, Pb, Se all = 0.01, analysed for mussels only Wet chemistry (“) - Hg = 0.01; As = 0.05

Test

Site

Table 2 Results of inorganic analyses of sediment and resident mussel samples in the Upper Waikato River

-

Y

.-

--7x*

,,

_, ,.,

170

C’. W: Hickey

et nl. / The Science

of the

only lo-fold in mussels (15.0-153 mg kgg ’ dry wt). There were no significant correlations between sediment total concentrations of either Hg or As and mussel tissue levels (I-\ = 0.33 and r, = 0.048, respectively, both P > 0.05). Norrnalisation of sediment concentrations for carbon or total iron did not increase the significant correlations. The absence of general relationships between mussel tissue and sediment concentrations for similar habitats suggests that differences in bioavailability may be influenced markedly by local site conditions. For example, the highest sediment As concentration (site W, 1520 mg kg- ’ ), was distant from known geothermal influences and was 3 to g-fold higher than sediment in adjacent lakes yet each of these lakes showed similar mussel tissue concentrations (15-23 mg kg- ’ >. The source of the high As is not known. Mussel bioaccumulation of Hg relative to sediment concentrations occurred at 4 of the 8 sites in the range 2-33-fold. Only the Taupo and Ohakuri mussels showed As bioaccumulation relative to sediment concentrations (8- and 1.4-fold, respectively). At other sites the sediment As exceeded mussel tissue concentrations by up to 38-fold (Fig. 2, Table 2). The mussel biomonitoring showed the extent of influence of bioavailable Hg and As on the Waikato River was limited to approximately 40-100 km (i.e., 1 or 2 hydrolakes?. The concentrations of other elements in mussel tissue generally showed a lower range than total concentrations in sediments (Table 2). The range in mussel tissue levels between sites exceeded 2-fold variation for: copper (Cu> (2.1-fold), calcium (Cal (2.3-fold), Co (2.7-fold), strontium (Sr) (2.8-fold), manganese (Mn) (3.1-fold), Cd (3.5fold), iron (Fe) (4.2-fold), Se (5.1-fold) and Pb (28-fold). The maxima for Pb, Cu, Co and Se occurred in Aratiatia, Ni in Ohakuri and Cd in Maraetai downstream. Pb, Co and Se showed a progressive downstream decline. Minima occurred for Sr, Fe and Mn at the high Hg site, Aratiatia. Sediment variability was maximal for Mn (37-fold), with highest Fe and Mn concentrations occurring at the highest As site, Waipapa. Copper, Cr and Co were maximal in Maraetai downstream (Md), the site located below a pulp

Total ~nt~irorment

I75 (1905)

163-I

77

and paper mill discharge. Elevated Hg, Cu, Co and Cr concentrations detected in the sediments in Maraetai downstream were at concentrations about 2-fold higher than the upstream site. The elevated Pb and Cu concentrations in the Aratiatia mussels is consistent with previous water measurements (Timperley, 1979) and may be attributable either to geothermal or sewage inputs. The elevated sediment Hg at Maraetai downstream may be attributed to losses from a chloralkali plant located at the pulp and paper mill site, which generated up until 1971 (Timperley, 1988). Elevated Cu and Cr in mussels and sediments at Maraetai downstream may also be associated with contaminants from timber treatment operations on the pulp and paper mill site. Resident mussels showed significant (P < 0.05) correlations between metals and Ca concentrations in tissue. Strong positive relationships occurred for Mg (T> = 0.81) and Fe (I, = 0.71) for all sites; for Se (rs = 0.96) excluding the highest Hg site (A); for Sr (r, = 0.86), Mn (rs = 0.821, P (r\ = 0.96) and Cu (rs = - 0.79) excluding the highest As site (0) and for Zn (rs = 0.94) excluding sites (A) and (0). Neither Hg or As showed a significant relationship with Ca concentration (rs = 0.26 and I-, = 0.57, respectively). The relationships with Ca accounted for most of the variability in the tissue concentrations of metals which is consistent with the deposition of metals in phosphatebearing extracellular granules (Jeffree and Brown, 1992). Similar granules have been observed in H. menziesi (authors’ observations). The Se level at the Hg elevated site (A) was markedly higher (approx. 5-fold) than relationships with Ca for other lake sites. However, tissue concentrations of Sr, Mn and P were lower at the As elevated site (0) suggesting possible competitive interactions. Metals (Cr, Cu and Mn) detected in both tissues and sediments showed no significant correlation between tissue and sediment concentrations, or with Fe or carbon normalised sediment concentrations. A significant positive correlation was observed for tissue Zn concentrations only when compared with total Fe normalised sediment metals (r, = 0.94, P < 0.05), but not for carbon normalisation (I; = 0.20, P > 0.1). This suggests that

C. W. Hickey

et al. / The Science

of the

iron may be affecting bioavailability. Tessier et al. (1984) found tissue concentrations of Cu, Pb and Zn in freshwater mussels was related to easily extracted sediment fractions and influenced by both iron oxyhydroxides and, to a lesser degree, organic matter. The levels of several metals exceeded sediment quality guidelines (Persaud et al., 1992) for Hg and As at most sites and for Cu, Cr, Fe and Mn at a few sites (Table 2). Hg exceeded the ‘Lowest Effect Level’ (LEL) at all sites except the most upstream (T) and downstream (H) sites, with all sites being below the ‘Severe Effect Level’ @EL). Sediment As exceeded the SEL at all sites except Taupo, indicating that the infaunal biota may be impacted. The mussel data, however, showed no correlation with sediment concentrations indicating that the bioavailability of the As was generally low. The levels of Cu and Cr exceeded the LEL in Maraetai downstream. These metals are probably derived from discharges and runoff from a sawmill which had previously operated on the pulp and paper mill site. At the next downstream site, Waipapa, Cu exceeded only the LEL but As, Fe and Mn levels all exceeded the SEL threshold. Although not commonly eaten, freshwater mussels are a traditional food of the indigenous Maori population of New Zealand (Hiroa, 1921). Mussel tissue concentrations exceeded the levels considered safe for human consumption for Hg and As. New Zealand Food Regulations (1984) standards for Hg (0.5 mg kg-’ wet wt for ‘fish and fish products’) was exceeded only in Aratiatia (circa 1 mg kg-’ dry wt). The As standard (2 mg kg ~ ’ 1 was exceeded for mussels at all sites sampled above Waipapa. The maximum Zn level was less than half the standard (40 mg kg- ’ 1, and Cu and fluoride levels less than 10% of the standards (30 and 15 mg kg-‘, respectively). These results suggest that consumption of shellfish may be limited by As in much of the Waikato River system, including the oligotrophic Lake Taupo. Timperley (1987) estimated that 17% of the dissolved solids in Lake Taupo were derived from geothermal water. The elevated mussel As is consistent with geothermal input to the lake.

Total EnL~ironment

175 (19951 163-I

77

171

The limited data available suggests that mussels may have lower levels of bioaccumulation than trout. Brooks, et al. (1976) reported trout flesh concentrations for Hg of 0.60 mg kg-’ (dry wt; 0.19 mg kg-’ wet wt) for Lake Taupo, which are 5-fold higher than the mussel concentrations (0.12 mg kg-’ dry wt>. An earlier study (Weissberg and Zobel, 1973) found similar concentrations of Hg in Taupo trout (0.2 mg kg-’ wet weight). Lake Maraetai has also been studied because of the high historic use of Hg by the pulp and paper mill. Cornposited sediment from downstream of the mill had a similar Hg concentration in this study (0.83 mg kg-’ 1, to the mean concentration measured by Weissberg and Zobel (1973) (0.89 mg kg- ’ >, whereas mussel levels were an order-of-magnitude lower than trout (0.08 cf. 0.70 mg kg-’ wet wt, respectively). Brooks, et al. (1976) measured flesh from 6 trout and found a mean concentration of 1.4 mg kg-’ wet wt. The differences in mussel and sediment Hg concentrations observed in this study and available trout data suggests that a greater understanding is required of the factors influencing Hg bioavailability and food chain transfer in this system. 3.2. Transplant eqeriments As H. menziesi can live > 30 years (Roper and

Hickey, 19941, accumulated body burdens in resident mussels could reflect historic contaminant levels. To assess present contaminant concentrations transplanted mussels from a common source were caged at the study sites. The rates of Hg and As uptake were measured using caged Taupo mussels transplanted down the river and the rates of depuration measured by transplanting Aratiatia (for Hg) and Ohakuri (for As) mussels to Taupo. Results are summarised in Table 3. The Hg uptake showed a progressive uptake with time in Aratiatia, with the 6 month concentration lofold higher than the Taupo mussels and amounting to 17-43% of the resident mussel levels (13.1 and 10.0 mg kg-’ 1. The Ulfvarson model (Ulfvarson, 1962, cited by Smith et al. (1975)) describes the uptake rate for Hg by simple linear regression, if the depuration rate of Hg were zero. Linear regression of the mussel Hg concentration

17’

C W. Hickey

et al. / The Science

of the

Total EnL!ironment

I75 (1995)

163-l

77

Table 3 Uptake of metals by caged mussels transplanted from Lake Taupo, and depuration of resident mussels transplanted to Lake Taupo Site

Incubation time months

As

Zn

Hg

cu

mg kg-’ DW

Ca gkg-‘DW

Uptake

Taupo Taupe Taupo Taupo

0 I 3 6

62.7

0.203

38.4 44.3 28.6,47.9, 33.4

267 202 155 219,235,238

6.2 7.9 5.0 8.2, 7.6, 6.6

19.7 14.9 16.6 18.9,21.8,18.7

0.206

Aratiatia Aratiatia Matiatia Matiatia

0 I 3 6

62.7 46.0 34.9 46.6,31.7, 45.6

0.203 0.590 1.30 2.07, 2.07 [5.51

269 232 365,179,277

11.4 9.1 13.1, 6.1, 9.3

19.7 19.7 13.4 21.5, 12.0, 18.1

Ohakuri Maraetai (upstream) Waipapa Hamilton

6 6

44.v 49.6

-

-

8.6

-

189

6 6

35.4 26.3

-

141 133

4.4 3.8

9.9 10.5

0 3 h 12

102.5 44 21 l32.31 -

10.0 10.2 9.8 5.9

-

-

Depuration”

Taupoh Taupoh Taupoh Taupoh

.

-

14.8

-

Note: Measurements from October 1990 unless noted. Metal concentration for composites of 8 mussels. All ICP analyses except Hg and As depuration. -. not determined. ‘Data from December 1991. ’ Deouration of resident mussels from Ohakuri for As and Aratitia for Hg transplanted to Taupo. ‘Taupe resident mussels at time of sampling caged mussels.

with time (mo) showed no deviation straight line regression:

from

a

mths”e = 0.31t + 0.27 (r = 1.0, n = 5, P = 0.005) This relationship indicates that the time required for transplanted mussels to reach the concentrations of Hg present in resident mussels (13 mg kg-‘, Table 2) would be 3.4 years. Smith et al. (1975) reported zero order uptake rate for Hg with the rate increasing in relation to water concentration, while Hg elimination was a function of its chemical form. Arsenic concentrations in mussels caged in Ohakuri were 44 mg kg-’ after 6 months, which compares with resident mussels from Ohakuri at

153 mg kg-’ (Table 3). The uptake did not differ significantly from the range measured in Taupo mussels. The low accumulation in Ohakuri may have resulted from the location of the cage 5 m above the bed and thus isolated from the natural lake sediments. Sediment As can be released to the water column under anoxic conditions (O’Brian, 1983), but the magnitude of the process at the current level of lake deoxygenation remains unknown. Accumulation of As in resident mussels may thus result from exposure to elevated concentrations by intimate association with the surrounding sediments and uptake of particulates or interstitial water, or by exposure to As rich hypolimnetic waters mixing with the epilimnion.

C. CK Hickey

et al. / The Science of the Total Enr:ironment

Caged mussels showed significant (P < 0.05) positive correlations between many elements (Sr, Zn, Fe. Mn, Mg, Se, S and P) and tissue Ca for the I,3 and 6 month incubation periods. Zinc and Cu increased in Aratiatia after 6 months by 18% and 27% respectively, however, these differences were not significant (P > 0.05). Calcium normalised Zn and Cu concentrations did, however, show significant increases compared with Taupo (1.3-fold, P < 0.1 and 1.5fold, P < 0.0001, respectively). The Ca normalised As data showed no significant differences. Neither Hg nor As showed a significant relationship with Ca concentration (rs = - 0.10, N = 5; and r, = 0.46, N = 14, respectively). Elevated Se concentration, as observed in resident mussels, was not apparent in transplanted mussels. Three composites of 8 randomly selected mussels showed coefficients of variation (0) of 27 and 20% for As determined for Taupo and Aratiatia respectively. It was found that the CV increased with higher downstream contaminant levels from 4 to 34% for Zn, 11 to 37% for Cu and from 8.8 to 28% for Ca (Table 3) though none of these differences were significant (Levene’s test of homogeneity of variance, P > 0.05). Water concentrations of Ca are similar throughout the upper Waikato River (Bryers, 19851, averaging 5.9 g rns3 at Taupo, 6.1 g mm3 at Ohakuri and 5.7 g m -’ at Hamilton and would not have been expected to have contributed to the wide range of Ca concentrations observed in the mussel composites. Differences in tissue Ca may have been caused by size differences in the mussels randomly selected for chemical analysis. Although there were no significant differences in shell weight, flesh weight or condition between caged mussels from Taupo or Aratiatia the shell wts used for Aratiatia condition measurements ranged from 51 g to 61 g, which may have provided sufficient range for tissue Ca differences. The levels of water Ca concentration have been shown to influence the rate of uptake of Cd (Wang and Evans, 1993) and Group II metals (Jeffree and Simpson, 1986). Waikato River Ca levels are about 40% of the world average freshwater concentration (Livingston, 1963). New Zealand river waters have been described as

175 (19951 163-l

77

173

‘calcium-sodium bicarbonate water’ to emphasise the nearly equal importance of Ca and Na among the cations (Close and Davies-Colley, 1990). The relatively low concentrations of Ca in New Zealand freshwaters would thus be expected to result in greater rates of metal uptake and potentially higher body burdens of metals in mussels compared with studies in hard waters. This may have consequences for adverse ecological effects on potentially sensitive life stages, such as glochidia, which have been shown to sequester maternal Ca (Silverman et al., 1987). Mercury and As depuration rates were investigated by transferring resident mussels to cages in Taupo. Tissue Hg depuration from Aratiatia mussels was relatively slow, with concentrations reducing to 60% of the initial levels after 12 months in Taupo (Table 3). Depuration of As from Ohakuri mussels transplanted to Taupo showed a progressive decline in concentration with tissue half-life of about 2.5 months (Table 3). These relatively slow rates of uptake and depuration indicate a longer time-integration period for metal contaminants which will reduce seasonal variation and increase the time required for the organism to show maximal physiological response and adaptation to metal contaminants. This finding of relatively long half-lives for metals in H. menziesi is consistent with other mollusc species and may be expected to contrast with much shorter half-lives found for organic pollutants (Phillips and Segar, 1986). 3.3. Bioconcentration

Mercury concentrations in the water column are estimated to increase 13.5-fold from the Lake Taupo outflow (0.2 pg rnp3) to Lake Aratiatia (2.7 pg rnp3) (Timperley, 1988; L. Bacon, Electricity Corporation of New Zealand, pers. comm.1, which compares favourably with a lo-fold increase in Hg concentration observed in the mussels (Table 3). The calculated bioconcentration factor for mussels in Aratiatia is circa 5 X 10h (dry wt basis). Bioconcentration factors for aquatic organisms are generally high (approx. 104), because of rapid uptake and slow elimination, with the biological half-life for Hg in fish approximately 2 years (CCREM, 1987). Mercury present

111

C. II/. Hickey

et al. /The

Science of the Total En~~ironment

in the mussels was as Hg” (J. Kim, NIWA Ecosystems, pers. comm.). This finding is surprising given that most of the Hg in trout mussel tissue is in the methyl form (Weissberg and Zobel, 1973). This suggests that the Hg exposure routes may differ markedly for mussels and trout in lakes receiving geothermal inputs. The low As levels in mussel tissue from Aratiatia compared with Taupo is surprising given the 3-fold increase in water As concentrations in this reach (from approx. 10 to 30 mg mm31 (Aggett and Aspell, 1980; Huser, 1991). Water concentrations show little increase to the outlet of Ohakuri, yet mussel tissue concentrations increase 6.5fold from Aratiatia to Ohakuri. Speciation measurements on two occasions showed that As (III) could range from 20-97% of total As in Aratiatia and 2642% in Ohakuri, suggesting that As (V) may be more readily bioaccumulated than is As (III). Recent studies have shown that total As concentrations in Aratiatia may vary daily from 30-160 mg me3 (L. Bacon, Electricorp, pers. comm.). The minimal bioaccumulation suggests that this As is not bioavailable compared with similar measured water concentrations in Ohakuri, and highlights a need for understanding speciation and cycling differences between these two lakes. 3.4. Physiological

measurements

A range of physiological parameters (condition, glycogen, protein, filtration rate and respiration rate) were measured in caged mussels to investigate potential influences of water-borne contaminants on mussel ‘health’. The caged mussels were used to provide a comparable population of mussels for each site. As freshwater mussels are a long lived species, 60 mm long corresponding to about 7 years (Roper and Hickey, 1994) the transplanted mussels would reflect current rather than historic conditions. The 6-month exposure period was known to be an adequate period within which marked responses in mussel condition and other physiological parameters could be expected (authors’ unpublished data). The physiological responses of the caged mussels encompassed sites having the major metal inputs. Resident and transplanted mussels in Ara-

I75 (1095)

163-I

77

tiatia with elevated tissue Hg showed a similar increase in condition compared with Taupo mussels (Fig. 3). Condition showed a general downstream increase for both caged (13%, P = 0.24) and resident mussels (56%, P < 0.05) in the reach from Taupo to Maraetai. The increase in mussel condition is consistent with the higher levels of food as indicated by chlorophyll a levels which increase 3-fold from the oligotrophic Lake Taupo to Lake Ohakuri (12-32 mg rnm3, (Huser, 1991)). Glycogen also showed a progressive downstream increase for caged mussels (38%, P = 0.431, while protein level and filtration rate showed no indication of downstream increases (P = 0.19 and 0.81). Both glycogen levels and filtration rate measurements were particularly variable between individual mussels. Respiration rate declined by 42% at Aratiatia compared with Taupo, with a statistically significant increase (109%, P < 0.05) to Maraetai. The physiological responses may be a response to increased food availability as a result of the discharge of Taupo sewage between the Taupo and the Aratiatia site, rather than a contaminant effect. Laboratory studies with mussels have shown respiration rate increases and filtration rate decreases in response to increased food levels (Roper and Hickey, 1995) Aratiatia resident and transplanted mussels had markedly different Hg levels yet each showed increasing condition relative to Taupo, suggesting that adverse impacts on adult mussels would not be expected to be marked. The slow uptake rate of Hg indicated that an incubation period of 3.4 years would be required to achieve tissue levels comparable with resident organisms. Organism responses have been shown to be related to whole-body residue concentrations (Connolly, 1985), thus maximum biotic responses may be expected only after equilibrium conditions have been obtained. These results highlight the need to understand biochemical changes induced by factors that are independent of environmental concentrations of contaminants, such as the influence of food levels, and the potential for metabolic adaptation in biomonitoring organisms. The caged mussels used, were of similar size (40-60 mm) corresponding to a median age of about 5 years (Roper and Hickey, 19941. At this stage the apparent growth rate of

C. W. Hickey

et al. /The

Science

of the

175 (1995)

16.3-177

175

the mussels is declining. The largest mussel recorded in the Waikato River was 84 mm which appeared to be 33 years old (Roper and Hickey, 1994). Thus during the 6-12-month incubation period effects related to growth would be unlikely. This study has shown that marked differences in contaminant concentrations and physiological responses may be detected after a &month incubation period. Hinch and Green (1989) found that tissue metal concentrations in transplanted mussels were a function of both the origin of the mussels and exposure environments. Such differences may be related to Ca levels in surrounding waters influencing metal accumulation (Jeffree and Brown, 1992; Wang and Evans, 1993) or to changes in food levels (Roper and Hickey, 1995). Thus different physiological responses might be expected for transplanted compared with resident mussels. The extent to which the origin of the organisms may inlhrence contaminant uptake and related effects is of particular importance for use of transplanted organisms to predict potential impacts on resident populations. An understanding of the ecological consequences of the measured physiological responses may require longer-term studies of reproductive effects to provide linkages with population responses.

0 25 20 15 10

70:

50

Total Emit-omnenr

L---J

Acknowledgements

The work has received funding from NZFP Pulp and Paper Ltd, Environment Waikato, Electricity Corporation of New Zealand and the Foundation for Research, Science and Technology (FRST). We thank J.B. Macaskill and an anonymous reviewer for their constructive review of an earlier draft of the manuscript and J. Kim for his Hg speciation data. References Aggett, J. and A.C. Aspell, 1980. Arsenic from geothermal sources in the Waikato catchment. New Zealand J. Sci., 21: Site Code Fig. 3. Physiological responses (means i: standard error) of resident mussels sampled October 1990 (condition only) (0) and caged mussels (6 months) and December 1990 to June 1991 ( q ). Sites are: Lakes Taupo (T), Aratiatia (A), Ohakuri (0) and Maraetai (upstream, Mu).

71-82.

Aggett, J. and M.R. Kriegman, 1988. The extent of formation of arsenic(III) in sediment interstitial waters and its release to hypolimnetic waters in Lake Ohakuri. Water Res., 22: 407-411. Axtmann, R.C., 1975. Environmental impact of a geothermal power plant. Science, 187: 795-803.

176

C. W Hickey

et al. / The Science of the Total Ent,ironment

Brooks, R.R., J.R. Lewis and R.D. Reeves, 1976. Mercury and other heavy metals in trout of central North Island, New Zealand. N.Z. J. Mar. Freshwater Res., 10: 233-244. Bryers, G.G., 1985. Water quality of Lake Taupo and the Waikato River - a general overview. In: Transport of carbon and minerals in major world rivers. Part 3. SCOPE/NNEP. pp. 525-537. CCREM, 1987. Canadian Water Quality Guidelines. Prepared by the Task Force on Water Quality Guidelines of the Council of Resource and Environment Ministers, Environment Canada, Ottawa, Ontario. Close. M.E. and R.J. Davies-Colley, 1990. Baseflow water chemistry in New Zealand rivers. 1. Characterisation. N.Z. J. Mar. Freshwater Res., 24: 319-341. Connolly. J.P., 1985. Predicting single-species toxicity in natural water systems. Environ. Toxic. Chem., 4: 573-582. Coughlan, J., 1969. The estimation of filtering rate from the clearance of suspensions. Mar. Biol., 2: 356-358. Elder, J.F. and J.J. Collins, 1991. Freshwater molluscs as indicators of bioavailability and toxicity of metals in surface-water systems. Rev. Environ. Contam. Toxicol., 122: 37-79. Farrington, J.W., A.C. Davis, B.W. Tripp, D.K. Phelps and W.B. Galloway, 1987. ‘Mussel Watch’ - Measurements of chemical pollutants in bivalves as one indicator of coastal environmental quality. In: T.P. Boyle (Ed.), New Ap proaches to Monitoring Aquatic Ecosystems. Philadelphia, American Society for Testing and Materials pp. 125-139. Goldberg, E.D., 1991. Halogenated hydrocarbons: past, present and near-future problems. Sci. Total Environ., 100: 17.-28. Hinch, S.G. and R.H. Green, 1989. The effects of source and destination on growth and metal uptake in freshwater clams transplanted among south central Ontario lakes. Can. J. Zool., 67: 855-863. Hiroa, T.R., 1921. Maori food-supplies of Lake Rotorua, with methods of obtaining them, and usages and customs appertaining thereto. Trans. R. Sot. N.Z., 53: 433-451. Huser, B.. 1991. Waikato River Water Quality Monitoring Programme. Waikato Regional Council. Technical Report No. 91/17. James, M.R.. 1985. Distribution, biomass and productian of the freshwater mussel, Hyridelia menziesi (Gray), in Lake Taupo. New Zealand. Freshwater Biol., 15: 307-314. Jeffrec, R.A. and P.L. Brown, 1992. A mechanistic and predictive model of metal accumulation by the tissue of the Australian freshwater mussel Velesunio an@. Sci. Total Environ., 125: 85-95. Jeffree. R.A. and R.D. Simpson, 1986. An experimental study of the uptake and loss of ‘2hRa by the tissue of the tropical freshwater mussel Velesunio angasi (Sowerby) under varying Ca and Mg water concentrations. Hydrobiologia, 139: i9--80.

Livingston, D.A.. 1963. Data of geochemistry, 6th edition, chapter G: Chemical composition of rivers and lakes. I!nited States Geological Survey professional paper 4Q)-G.

175 (1995)

163-177

H.W., 1983. Determination of total mercury in fish: an improved method. Analyst, 108: 1313-1317.. Martin, M. and R. Severeid, 1984. Mussel watch monitoring for the assessment of trace toxic constituents in California marine waters. In: H.H. White (Ed.), Concepts in Marine Pollution Measurements. Maryland Sea Grant College, University of Maryland. pp. 291-324. Millington, P.J. and K.F. Walker, 1983. Australian freshwater mussel Velesunio ambiguus (Philippi) as a biological monitor for zinc, iron and manganese. Aast. J. Mar. Freshwater Res., 34: 873-892. O’Brian, G.A., 1983. Observations on the mobility of arsenic in the sediments of Lake Ohakuri. Ph.D. Thesis. University of Auckland Library, Auckland, N. Z., pp. 257. O’Connor, T.P., 1992. MusseI watch: recent trends in environmental quality. U.S. Department of Commerce, National Oceanic and Atmospheric Administration. Persaud, D., R. Jaagumagi and A. Hayton, 1992. Guidelines for the protection and management of aquatic sediment quality in Ontario. Ontario Ministry of the Environment. 92-2309-067. Phillips, D.J.H. and P.S. Rainbow, 1992. Biomonitoring of trace aquatic contaminants. Elsevier Applied Science, London. Phillips, D.J.H. and D.A. Segar, 1986. Use of bio-indicators in monitoring conservative contaminants: programme design imperatives. Mar. Poll. Bull., 17: 10-17. Pickston, L., J.F. Lewin, J.M. Drysdale, J.M. Smith and J. Jane, 1983. Determination of potentially toxic metals in human livers in New Zealand. J. Anal. Toxicol., 7: 2. Roper, D.S. and C.W. Hickey, 1994. Population structure, shell morphology, age and condition of the freshwater mussel I@idella menziesi (Unionacea: Hyriidae) from seven fake and river sites in the Waikato River system. Hydrobiologia, 284: 205-217. Roper, D.S. and C.W. Hickey, 1995. Effects of food and silt on filtration, respiration and condition of the freshwater mussel Hyrideila menziesi (Unionacea: Hyriidae): implications for bioaccumulation. Hydrobiologia, in press. Ryan, S., G.J. Bather and A.A. Martin, 1972. The mussel Hyridella australis as a biological monitor of the pesticide endrin in fresh water. Search, 3: 446-447. Silverman, H., W.T. Kays and T.H. Dietz, 1987. Maternal calcium contribution to glochidial shells in freshwater mussels (Eulamelhbranchiata: Union&e). J. Exp. Zool., 242: 137-146. Smith, A.L., R.H. Green apd A. Lutz, 1975. Uptake of mercury by freshwater clams (family Unionidae). J. Fish. Res. Board. Can., 32: 1297-1303. Snedecor, G.W. and W.G. Cochran, 1980. Statistical methods. The Iowa State University Press. Ames, Iowa, U.S. Sokal, R.R. and F.J. Rohlf, 1981. Biometry. 2nd. W.H. Freeman, New York. Tess&, A., P.G.C. Campbell, J.C. A&air and M. Bisson. 1984. Relationships between the partitioning of trace metals in sediments and their accumulation in the tissues of L.ouie,

C. W. Hickey et al. /The Science of the Total Environment 175 (1995) 163-177 the freshwater mollusc Elliptio complanuta in a mining area. Can. J. Fish. Aquat. Sci., 41: 1463-1472. Timperley, M.H., 1979. Metals in the water of the Waikato River, New Zealand. N.Z. J. Sci., 22: 273-279. Timperley, M.H., 1987. Regional influences on lake water chemistry. In: A.B. Viner (Ed.), Inland waters of New Zealand. Wellington. DSIR Science Information Publishing Centre, pp. 97-l 11. Timperley, M.H., 1988. Mercury in the Waikato River. Proceedings of The 10th New Zealand Geothermal Workshop 1988, Auckland, pp. 235-238. UlfLarson, U., 1962. Distribution and excretion of some mercury compounds after long term exposure. Int. Arch. Gewerbepath. Gewerbehyg., 19: 412-422.

177

Viarengo, A. and L. Canesi, 1991. Mussels as biological indicators of pollution. Aquaculture, 94: 225-243. Walker, K.F., 1981. The distribution of freshwater mussels (Mollusca: Pelecypoda) in the Australian zoogeographic region. In: A. Keast (Ed.), Ecological Biogeography of Australia. The Hague, Junk Publishers, pp. 1233-1249. Wang, Y. and R.D. Evans, 1993. Influence of calcium concentrations on cadmium uptake by the freshwater mussel EIliptio complanuta. Can. J. Fish. Aquat. Sci., 50: 2591-2596. Weissberg, B.G. and A.G. Rohde, 1978. Mercury in some New Zealand geothermal discharges. N.Z. J. Sci., 21: 365-369. Weissberg, B.G. and M.G.R. Zobel, 1973. Geothermal mercury pollution in New Zealand. Bull. Environ. Contam. Toxicol., 9: 148-155.