Marine Pollution Bulletin, Vol. 30, No. 10, pp. 646-654,1995
Copyright 0 1995 Elsevier Science Ltd
Printed in Great Britain. All rights reserved
0025-326X(95)00039-9
Pergamon
0025-326X/95 $9.50+0.00
Contaminants in Oysters in Kaneohe
Bay, Hawaii
CYNTHIA L. HUNTER*TI, MARK D. STEPHENSONt,
RONALD S. TJEERDEMAS,
DONALD G. CROSBY& GARY S. ICHIKAWA_F, JON D. GOETZLt, KIM S. PAULSON?,
DAVID B. CRANEt, MICHAEL MARTINI_ and JOHN W. NEWMANS
*Hawaii Institute of Marine Biology, University of Hawaii, Kaneohe, HI %744, USA
j-Marine Pollution Studies Lab, California Department of Fish and Game, Moss Landing, CA 95930, USA
$-Department of Chemistry and Biochemistry and Institute of Marine Sciences, University of California, Santa Cruz,
CA 95064, USA
SDepartment of Environmental Toxicology, University of California, Davis, CA 95616, USA
llPresent
address:
Department
of Botany, University
of Hawaii, Honolulu,
Despite past and present concerns about the toxicity
and persistence of various environmental contaminants
(heavy metals and pesticides), relatively few studies
have documented their concentrations
in tropical or
sub-tropical marine ecosystems. In this investigation, a
‘mussel watch’ approach was applied in Kaneohe Bay,
Hawaii, to assess the present levels of potential contaminants
in the Pacific oyster, Cmssostrea gigas.
Geographical gradients of these contaminants
were
observed and related to what is known about past and
present
inputs.
Concentrations
of lead, copper,
chromium and zinc were elevated in oyster tissues near
stream mouths in the southern watersheds of Kaneohe
Bay. Dieldrin and chlordane concentrations in oysters
from one of these sites exceeded the US Environmental
Protection Agency’s screening levels to protect human
health, and were much higher than in oysters from the
east and Gulf coasts of the temperate mainland USA.
Numerous studies have documented the accumulation
of contaminants in benthic sediments and biota near
industrialized areas or dense population centres at
temperate latitudes (Goldberg et al., 1978; Stephenson
et al., 1979; Phillips, 1980; NOAA, 1989). Studies in
tropical and sub-tropical
environments
have been
limited, but indicate similar elevations of contaminants
in marine ecosystems receiving run-off from lands used
for agricultural purposes or near heavily populated
locations (Olafson, 1978; Menasveta & Cheevaparanapiwat, 1981; Brown & Holley, 1982; Glynn et al.,
1984, 1989; Hallecher et al., 1985; Paez-Osuna et al.,
1986; Dougherty, 1988; Hungspreugs, 1988; Phillips,
1991; Guzman & Jimenez, 1992). Although previous
investigations demonstrate the presence of high concentrations of toxicants in some tropical regions, the
distributions of these toxicants are poorly understood
in most areas.
Pesticide contamination in Hawaiian biota was first
documented in 1969 (State of Hawaii, 1969). In a
646
HI 96822,
USA.
nationwide survey of pesticides in freshwater fish,
Hawaiian samples rated highest in dieldrin and
chlordane concentrations between 1970 and 1974 and
again between 1976 and 1979 (Schmitt et al., 1981,
1983). A more recent study indicated that bivalves
(Ostrea spp.) collected within Hawaiian harbours and
ports contained very high concentrations of a number
of contaminants compared to bivalves from US mainland coasts (NOAA, 1989). However, accumulation of
metals and organic pesticides in marine bivalves may be
species-specific as shown by differential accumulations
among species with overlapping ranges. Therefore, the
high concentrations
of contaminants
in Hawaiian
Ostrea were cautiously interpreted
(NOAA, 1989).
Because little information currently exists describing
concentrations of toxic substances in tissues of Ostrea
spp. from locations outside Hawaii, we analysed tissues
from Crassostrea gigas for direct comparison with other
studies and to determine if the trends in contaminants
observed for Ostrea spp. may reflect those of other
bivalves in other habitats in Hawaii.
Kaneohe Bay, Hawaii, has served as a model for
identifying the impacts of urbanization on tropical
Pacific ecosystems (Smith et al., 1973, 1981). The
surrounding watersheds underwent a 2000% increase
in population size between 1940 and 1990, and the
south end of the bay received municipal sewage discharges from the mid-1960s through to the late 1970s.
Since sewage discharge was diverted from the bay in
1977-1978,
there have been only rare (accidental)
point-source discharges into bay waters. The potential
for introduction of contaminants through non-point
source run-off from urbanized watersheds of the
southern bay and from rural-agricultural areas of the
central and northern bay was last evaluated in 1975
(Young et al., 1976). Fate and persistence of toxicants
in bay biota have not been addressed previously. A
recent workshop aimed at identifying research needs
for coastal ecosystems in the bay concluded that very
little was currently known about contaminants
in
Hawaii in general, and in Kaneohe Bay specifically.
Volume 30/Number
lo/October
1995
We used a ‘mussel watch’ approach to assess the
current concentrations of metals and pesticide residues
in Kaneohe Bay. This approach has been used in Hong
Kong (Phillips, 1980), Australia (Phillips, 1976) and the
et al, 1978, 1983;
temperate
USA (Goldberg
Farrington et al., 1983; Martin & Castle, 1984; Smith et
al., 1986; NOAA, 1989) to assess contaminant concentrations.
Our study involved the collection of
samples of Pacific oysters (C. gigas) along a northsouth gradient reflecting the urbanization of watersheds
surrounding the bay, analysis of the extracts for
contaminants, and comparison of results to those from
other areas. Crassostrea gigas, a bivalve mollusc introduced to Kaneohe Bay in 1939 (Kay, 1979) was chosen
as a bioindicator because of its relative abundance
throughout the bay and to allow direct comparison with
published findings for this species at other tropical and
temperate localities. Our goals were to establish a
toxicant baseline for bay biota and to determine the
potential for toxicant stress on the surrounding
estuarine and coral reef environments of Kaneohe Bay.
Methods
Collections and dissections
Sample sites were selected to bracket the range of
Map Of
Kaneohe Bay
/!
!
Arsenic
environmental gradients in Kaneohe Bay, with a focus
on the southern (more urbanized) region of the bay. We
collected Pacific oysters from five stations during the
period of June to September, 1991 (Fig. 1): Makani Kai
Marina, Kaneohe Stream and the Marine Base on 28
June 1991, Lilipuna Pier on 6 August 1991, and
Waikane on 27 September 1991. Attempts were made
to collect samples of similar size (5-10 cm shell length)
and from the same tidal height (mean low water) at each
site.
Oysters were pried from the substratum with
stainless-steel diving knives, placed in polyethylene
bags, and frozen at -10°C until dissection. Twenty-one
oysters (three replicates of seven oysters each) were
collected from each of four study areas: 18 oysters
(three replicates of six oysters each) were collected from
the Marine Base site. Samples were thawed and dissected with stainless steel scalpels in a positive-pressure
clean-air room previously tested for contamination
(Stephenson et al., 1979). Oysters were dissected into
acid- and solvent-rinsed glass jars with Teflon-lined
lids. Whole bodies (soft tissues) were homogenized
individually with a Brinkman tissue homogenizer
equipped with a titanium shaft cleaned with detergent,
methanol, petroleum ether, and trace metal and trace
organic-free
Milli-Q deionized water before each
homogenization.
_)
Zinc
Kaneohe Stream
Copper
Chromium
Fig. 1 Collection locations and relative concentrations of metals (pg
g-l dry wt) in whole tissue extracts of Crussostrea gigas in
Kaneohe Bay, Oahu, Hawaii.
647
Marine Pollution Bulletin
TABLE 1
Trace metal digestion and analysis
For each of the three replicates, 3 g of wet tissue was
digested for 4 h in 3 ml of a 4:l mixture of ultra-pure
nitric and perchloric acids (Fisher Ultima Grade) at
130°C in Teflon” digestion vessels. Samples were
cooled, diluted to 20 ml, and transferred to acidcleaned polyethylene bottles for analysis. We determined Ag, As, Cd, Cr, Pb and Se concentrations by
graphite furnace atomic absorption spectrophotometry
(Perkin-Elmer Model 3030 with Zeaman background
correction); Cu, Mn and Zn were determined by flame
atomic absorption spectrophotometry
(Perkin-Elmer
21280). All results were expressed on a dry weight
basis.
Organic extraction and analysis
For analysis of organic contaminants, aliquots of
tissue from each of the three homogenized replicates
were combined into a single sample for each site in
order to minimize costs. Two different analytical
procedures were used. Samples from Kaneohe Stream
were analysed for selected pesticides and PCBs by the
method described in MacLeod et al. (1985) at the
University of California, Santa Cruz. After this initial
screening, samples from the other four stations were
analysed using the US Food and Drug Administration
(USFDA, 1975) method by the California Department
of Fish and Game. The USFDA method is specific for
more pesticides than that of MacLeod et al. (1985). The
method of MacLeod et al. (1985) pooled 3.3 g from
each of the three replicates into one 10 g sample for
extraction. The USFDA method utilized 13.3 g from
each of the three replicates pooled into one 40 g
sample. Since replicate analyses were not performed,
concentrations
of organic compounds were not subjected to statistical tests. Compounds analysed and the
detection limits for both methods are presented in
Table 1.
Quality controUassurance
The University of California, Santa Cruz, and
California Department of Fish and Game analytical
laboratories are participants in the National Oceanographic and Atmospheric
Administration
National
Status and Trends trace metal and trace organics
intercalibration
programme (Cantillo & Lauenstein,
1992). The two organic methods were compared for
several pesticides, giving the following results for the
MacLeod and USFDA methods, respectively: chlordane, 48.2 ng g-’ and 54.5 ng g-l; dieldrin, 45.0 ng g-’
and 36.5 ng g-l; DDE, 18 ng g-l and 23 ng g-l; and
PCB-1254, 200 ng g-’ and 215 ng g-l. These results
indicate that good agreement exists between these
testing procedures. In addition, two separate analyses
were conducted on the pooled sample from the Marine
Base site as a within-method control (Marine Base-
QC).
Results
Levels of present or historical inputs of metals and
pesticides into Kaneohe Bay waters are reflected by the
648
Detection limits of synthetic organic compounds and trace elements
analysed in this study on a dry weight basis.
Compound
Aldrin
cis-Chlordane
truns-Chlordane
a-Chlordene
y-Chlordene
Chlorpyrifos
Dacthal
o,p’-DDD
p,p’-DDD
o,p’-DDE
p,p’-DDE
p,p’-DDMS
o,p’-DDMU
o,p’-DDT
p,b’-DDT
Dieldrin
Endosulphan sulphate
Endrin
a-HCH
P-HCH
y-HCH
8-HCH
Heptachlor
Heptachlor epoxide
cis-Nonachlor
trans-Nonachlor
Oxychlordane
Parathion, ethyl
Parathion, methyl
PCB 1248
PCB 1254
PCB 1260
Detection
limit
(ng g-9
1
1
1
1
1
4
2
5
3
3
3
20
Trace element
Arsenic
Cadmium
Chromium
Copper
Lead
Manganese
Selenium
Silver
Zinc
Detection
limit
(CLgg-9
0.57
0.008
0.03
0.04
0.1
0.08
0.5
0.002
0.4
4
50
6
0.8
2
10
4
50
10
10
relative concentrations
of these contaminants in the
oyster samples from various parts of the bay (Tables 2
and 3; Fig. 1). Concentrations of metals and pesticides
varied along the north-south urbanization gradient of
the bay. Lead concentrations were ten-fold higher in
oysters at the south end of the bay near Kaneohe
Stream and Makani Kai Marina than at the station in
the north near Waikane Stream (Fig. 1). Multiple
comparison statistical tests (Tukey’s test; Wilkinson,
1989) indicated
that concentrations
of copper,
chromium, lead and zinc were significantly higher at
Makani Kai Marina than Waikane Stream.
In general, concentrations
of arsenic, copper,
chromium and lead were moderate to high in Kaneohe
Bay oysters, while cadmium, and zinc concentrations
were low when compared with other studies of metals
in C. gigas (Table 4). Although interspecies comparisons should be cautiously interpreted because of
the variability in accumulation rates of metals among
some bivalve species (NOAA, 1989), Table 4 shows
that concentrations of metals in C. gigas are generally
similar to those reported from other species and genera
from different geographic areas. The metal concentrations that we found in C. gigas from Kaneohe Bay were
also remarkably similar to those reported from Ostrea
spp. collected from three Hawaiian harbours (NOAA,
1989).
Concentrations of DDT, PCBs, and other organic
pesticides assayed in this study were low or undetectable (Table 3). However, chlordane and dieldrin
Volume 30/Number
lo/October
1995
TABLE 2
Oyster size (x* SE) and concentration of metals in whole body tissue (pg g-l dry wt, x* SE) of Crassostrea gigas from five sites in Kaneohe
Bay, Hawaii.
Oyster
length
(mm)
Sites
Oyster
weight
(g)
Metals
As
Ag
Cd
cu
Cr
Mn
Pb
Se
Zn
Marine Base
91.11
f 4.95
98.30
i? 7.65
11.87
f 1.84
7.05
f 1.51
0.61
f 0.05
165.20
f 13.86
2.57
f 0.49
13.41
f 2.62
0.60
+0.11
3.41
f 0.32
854.46
+ 98.93
Kaneohe Stream
68.57
f 2.35
36.50
f2.16
8.47
f0.51
7.28
f0.53
0.54
f 0.04
335.43
zt 35.25
10.01
+ 2.47
14.68
f 1.73
0.99
f 0.09
2.88
kO.14
544.60
It 43.03
Makani Kai Marina
55.24
f3.13
27.80
f 2.69
8.54
* 1.45
5.68
* 1.00
0.61
f 0.03
522.33
k45.81
6.47
+ 2.02
14.68
* 1.07
1.76
* 0.57
3.06
f0.21
1211.27
!c 56.34
Lilipuna Pier
52.62
f2.17
26.40
f 1.13
11.61
* 0.44
9.35
f 1.36
0.57
f 0.02
244.86
f 33.41
4.42
+ 1.22
14.45
f 0.97
0.43
f 0.02
3.00
f 0.54
591.55
* 74.53
Waikane Stream
73.00
* 3.5
52.40
f 4.60
13.70
f 0.35
6.32
f 0.09
0.69
fO.ll
333.75
? 87.02
2.03
* 0.21
12.06
zt5.12
0.10
+ 0.06
3.26
f 0.22
600.94
f 155.14
TABLE 3
Levels (ng g-t dry wt) of organic toxicants in oysters from five sites in Kaneohe Bay.
Waikane
Stream
Lilipuna
Pier
Makani Kai
Marina
cis-Chlordane
trans-Chlordane
Oxychlordane
cis-Nonachlor
rrans-Nonachlor
a-Chlordene
y-Chfordene
Heptachlor
Heptachlor epoxide
Sum of chlordanes
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
8
5
ND
ND
ND
ND
ND
ND
ND
13
88
75
5
46
32
ND
15
ND
29
290
Aldrin
Chlorpyrifos
Dacthal
Dieldrin
o,p’/p,p’-DDD
o,p’/p,p’-DDE
p,p’-DDMU
o,p’/p,p’-DDT
Endosulphan sulphate
Endrin
a-, 8-, y-, &HCH
Parathion, ethyl
Parathion, methyl
PCB 1248
PCB 1254
PCB 1260
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
10
ND
ND
ND
ND
ND
ND
ND
17
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
200
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
Toxicants
ND-Not
Kaneohe
Stream
36
30
4.1
25
42
ND
2.2
7.4
ND
147
ND
ND
ND
92
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
57
ND
Marine
Base
Marine
Base Q.C.
7
5
ND
ND
ND
ND
ND
ND
ND
7
5.2
ND
ND
ND
ND
ND
ND
ND
12
12.2
ND
ND
ND
7.6
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
52
ND
ND
ND
ND
7.5
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
57
ND
detected.
300
Chlordane
1
Dieldrin
J
Fig. 2 Relative concentrations (ng g-l dry wt) of chlordane and
dieldrin in Crussostreu gigas from Kaneohe Bay compared to
NOAA (1989) National Status and Trends 90% limits (NS&T
90%) and highest levels (NS&T highest) reported from
mainland US oyster samples.
concentrations
represented the highest reported for
these pesticides in any bivalve population sampled from
the eastern or south-eastern
US mainland by the
National Status and Trends Program (Table 5; Fig. 2).
Mean lengths and weights were significantly smaller
for oysters collected at Makani Kai and Lilipuna Pier
than for the three other sites (Table 2; Tukey’s test;
Wilkinson, 1989). The oysters with largest mean sizes
(Marine Base) had generally lower concentrations of
contaminants, indicating that high levels of toxins were
not related to larger body sizes in these bivalves.
Discussion
Over the past century, the watersheds surrounding
Kaneohe Bay have been utilized for a succession of
agricultural activities (primarily taro, rice, pineapple,
649
me
me
me
cr
as
Pv
ci
cc
cc
SC
OS
OS
OS
cv
cv
cv
cg
cg
%
cg
cg
cg
cg
cg
Species*
1-18
5.3-10.9
0.3.5-3.6
1.5
1.2
0.012
0.58
0.12
Ag
16
18
8
0.5-5.5
0.5-22.5
1.2-l 3.9
6.1-14
27
15
6
5.8-9.0
11
8.2
12
As
1.2
0.81
0.35
4-135
J-23
2.0-5.5
3.0-27.0
0.5-0.8
1.4-8.4
2.9
0.36
5
46-62
2.6
2.0-15.9
2.9-4.1
0.75-1.3
0.5-2.5
0.4-2.7
2.1-3.8
6
0.07
Cd
-, Not analysed.
cucullata; OS, Ostrea spp.
0.15-0.24
0.24-0.59
2.8-4.0
1.9
2.3
8.2
1.8-11.5
0.17-0.67
0.51
0.21
1.8
7.5-9.3
0.87
l-37
0.17
Cr
2.3
4.9
0.77
o-135
O-30
0.5-2.0
OS-O.4
0.04-2.4
0.28-0.63
0.22
0.28
0.53
3.9-7.1
1.3
0.6-l 5.6
1.7-7.3
6.9-l 5.3
0.1-1.0
0.5-13.1
2.1
Pb
Zn
SC, Saccostrea
Thornton et al. (1975)
Hiraoka (1991)
Pridmore et al. (1990)
Ayling (1974)
Thomson (1982)
Phillips et al. (1982)
Phihips et al. (1982)
Present study
NOAA (1989)
NOAA (1989)
NOAA (1989)
NOAA (1989)
Okazaki & Panietz (1981)
NOAA (1989)
campos (1988)
Leavitt et al. (1989)
Chart (1989)
Soria & Theede (1990)
Hungspreugs (1988)
Phillips & Muttarasin (1984)
Dougherty (1988)
NOAA (1989)
NOAA (1989)
NOAA (1989)
Reference
iredale; cc, Crassostrea commercialis;
790
840
620
64-85
74-96
1000-4000
83-1256
571-1048
1640
740
970-4146
2000-14000
200-7800
1200-3310
1345-3110
422-1268
1200-4500
1400
2200
89
4514-6219
150
az, Area zebra; pv, Pema viridis; ci, Crassostrea
273
140
178-1219
200-1700
lo-380
220-1270
550-l 545
151-525
30-250
64
90
5.4
1241-1680
5.6
5.9-91.7
5.7-9.8
17-158
20-100
6-276
loo-181
70-160
1200
1400
700
cu
Metals
*Species abbreviations: cg, Crassostrea gigas; cv, Crassostrea virginica; me, Mytilus edulis; cr, Crassostrea rhizophorae;
Helford, UK
Hiroshima Bay, Japan
Manukau Harbour, New Zealand
Tamar River, Tasmania
Southern Tasmania
Deep Bay, Hong Kong
Retail market, Hong Kong
Kaneohe Bay, Hawaii
Chesapeake Bay, Maryland
Savannah River, Georgia
Biscayne Bay, Florida
Tomales Bay, California
San Francisco, California
Mission Bay, California
Caribbean coast, Colombia
Poll. gradient, Bermuda
Poll. gradient, Hong Kong
Manila Bay, Philippines
Upper Gulf, Thailand
Upper Gulf, Thailand
11 sites, Fiji
Barbers Point, Hawaii
Honolulu Harbor, Hawaii
Kauai, Hawaii
Location
TABLE 4
Metal concentrations (ug g-r dry wt) in bivalves reported from various studies.
Volume
30/Number
lo/October
1995
TABLE 5
Concentration
of organic
toxicants
Organic
Location
Temperate sites
Chesapeake Bay, Maryland
Savannah River, Georgia
Tomales Bay, California
Mission Bay, California
Baja California, Mexico
Tamar River, New Zealand
Manukau Harbour, New Zealand
Tropical sites
Malaysia
Philippines
Thailand
India
Benin Bight, Nigeria
Biscayne Bay, Florida
Mazatlan, Mexico
Hawaii Kai Marina, Hawaii
Honolulu Harbor, Hawaii
Barber’s Point, Hawaii
Kauai, Hawaii
Kaneohe Bay, Hawaii
*
Speciest
cv
CV
*
*
*
*
*
*
*
*
me
me
cg
cg
cg
E Chlordane
21-51
12
3.3
20
_
_
in bivalves reported
concentrations
in various studies.
(ng g-‘)
Dieldrin
ZDDT
PPCB
5-22
5.9
3.5
3.2
31-100
13
15
70
4-65
50-300
21-60
72-390
46
34
310
22-66
16-78
25-126
‘Shellfish’
‘Oysters’
5-25
13.5
130-2.50
_
135-220
_
Pv
Pv
ca
cv
cc
‘Oysters’
OS
OS
OS
50
120
14-200
91-138
45
18-22
5-388
23
22
36
8-10
50
3-36
122-387
210
6-7
220
230
220
52-57
cg
28
_
12-288
26
19
13
12-261
17
_
2-127
7.2
8.2
1.5
8-200
Reference
NOAA (1989)
NOAA (1989)
NOAA (1989)
NOAA (1989)
Cajal-Medrona
& Gutierrez-Galindo
Sumner (1978)
Pridmore et al. (1990)
(198 1)
Hungspreugs
(1988)
Hungspreugs
(1988)
Hungspreugs
(1988)
Ramesh et al. (1990)
Osibanjo & Bamgbose (1990)
NOAA(1989)
Martin & Gutierrez-Galindo
(1989)
Tanita et al. (1976)
’
NOAA (1989)
NOAA j1989j
NOAA(1989)
Present study
*Conversion from wet to dry weight values; conversion factor = X 5.
tSpecies abbreviations:
cv, Crassostrea virginica; me, Myths edulis; cg, Crassostrea gigas; pv, Perna viridis; ca, Crassostrea gasar; cc, Crassostrea
corteziensis; os, Ostrea spp.
-, Not analysed.
sugarcane, cattle grazing, truck farming and horticulture), military operations (Kaneohe Marine Corps
Air Station), and urban development
(residential
housing, golf courses, cemeteries, marinas, shopping
centres and small businesses) (Devaney et al., 1982).
The potential for contamination of Kaneohe Bay waters
and associated marine life by toxic residues from these
various land uses is reflected by the preliminary
screening of metals and pesticides reported here.
Northern watersheds that drain into Waikane Stream
are characterized primarily by rural and small-scale
farming land uses. Oysters from this stream mouth
showed detectable concentrations of parathion, but low
concentrations
of other contaminants.
In contrast,
oysters from the mouth of Kaneohe and Makani Kai
Marina, the major outlets of drainages from the
southern (urbanized)
watersheds,
had high tissue
concentrations
of lead, copper, chromium and zinc.
These metals are common contaminants associated
with automobiles (batteries and gasoline (Pb); plating
(Cr); tyres (Zn)), residences in Hawaii (wood preservation and banana fumigation (Cu)), and small boat
marinas (Cu).
The high concentrations of chlordane and dieldrin
found in oysters in the southern bay samples may be the
result of long-term accumulation in tissues or sediments, although recent (illegal) application of these
banned pesticides cannot be ruled out. Tissue concentrations of dieldrin in Kaneohe Bay were similar to
those found in C. gigas in California near agricultural
areas during the mid-1960s when dieldrin was still in
use for agricultural purposes (Moden, 1969). Chlordane was banned in the USA in 1978, except for
underground termite treatment; all uses were cancelled
in 1988 (Eisler, 1990). Dieldrin usage was cancelled by
the USEPA in 1987. The most recent available usage
levels in Hawaii were approximately
58 000 kg
chlordane and 236 kg dieldrin in 1977, down from
64 000 kg and 7300 kg, respectively, in 1968 (State of
Hawaii, 1969; Takahashi, 1982). The principal users of
both compounds were pest control operators.
The half-life of chlordane is 350 days; that of
dieldrin is approximately 3 years. However, isomers
and breakdown products may be much more persistent
(e.g. 3-14 years for chlordane in soils (Eisler, 1990))
because of low solubility in water, high solubility in
lipids and low vapour pressure of these compounds.
The USEPA (1993) has recently issued ‘screening
values’ for various toxicants based on estimated human
consumption rates. Concentrations in excess of these
values ‘should be taken as an indication that more sitespecific monitoring and/or evaluation of human health
risk should be conducted’ (USEPA, 1993). For
chlordane, screening values are 400, 205 and 19 ng g-i
dry weight for adults, children, and subsistence
fishermen, respectively. The Makani Kai Marina oysters
(290 ng g-i) exceeded screening values for the latter
two groups. Dieldrin screening values are 35, 18 and
1.5 ng g-i for adults, children, and subsistence
fishermen, respectively; values for all groups were
exceeded by the Makani Kai Marina dieldrin tissue
concentrations of 200 ng g-l.
Concentrations
of metals and pesticides were
measured in Kaneohe Bay streams and bay waters in
1975 (Young et al., 1976). Metals concentrations in the
bay were again analysed in 1989 (Hawaii Department
of Health, unpublished data). Concentrations
of dissolved metals in seawater for various sites in Hawaii,
including the two samplings of Kaneohe Bay, are
presented for comparative purposes in Table 6. It is
651
Marine Pollution Bulletin
clear that metal concentrations measured in Kaneohe
Bay seawater in 1975 were extremely low. Whether
these low values were due to low detection/recovery
of
the samples or lower absolute values of metals input to
the bay is not clear, but the 1975 values were comparable to those reported for other coastal waters near
urbanized areas in Hawaii during that period (Young et
al., 1976). More recent reports indicate that some
metals in Kaneohe Bay seawater (e.g. Pb, TBT) may
exceed Hawaii Department of Health limits.
Concentrations of metals in sediments in Kaneohe
Bay showed an accumulation of approximately 0.5-2
orders of magnitude over concentrations in seawater
(Tables 6 and 7). Relative concentrations of metals in
bay oysters did not directly correspond with those in
sediments. Arsenic and copper in C. gigus tissues from
Kaneohe Bay were three to five times greater than the
reported sediment concentrations; silver concentrations
were more than two orders of magnitude greater. In
contrast, chromium and lead were one to two orders of
magnitude less concentrated in oyster tissues compared
to their levels in sediments.
Of the organic pesticides measured in seawater in
1975 (Young et al., 1976), only chlordane, dieldrin and
PCP were detected, and only at low (pg g-l) concentrawere somewhat
higher in
tions. Concentrations
Kaneohe Stream (8.6 pg g-l chlordane and 9.0 pg g-l
dieldrin) than in Waikane Stream (2.8 pg g-l chlordane
and 1.1 pg g-l dieldrin), reflecting the impact of the
termiticides in the urbanized vs rural watersheds. More
recent published values for levels of pesticide input into
Kaneohe Bay waters are not available, nor are there
estimates of input of the dozens of pesticides in use but
not analysed in the present study.
The toxicological or ecological impacts of metals and
pesticides on the estuarine and coral reef communities
of Kaneohe Bay have not been determined. Pridmore et
al. (1991) found that low concentrations of chlordane
added to natural sediments caused rapid and significant
changes in the population structure and densities of two
temperate bivalve species. High concentrations (pg g-l)
of pesticides and metals were found in corals and
octocorals in Florida (Glynn et al., 1989), but these reef
populations showed no significant differences in health
characteristics between ‘polluted and ‘non-polluted’
sites. Red Sea reef corals concentrated higher levels of
heavy metals in soft tissue and skeleton in polluted
areas relative to unpolluted areas (Harma & Muir,
1990). The larvae of a scleractinian coral (Pocilloporu
dumicornis) are sensitive to very high levels of nickel,
carbaryl, naphthol and chlorpyrifos, although larvae are
surprisingly tolerant of lower concentrations (Acevedo,
TABLE 6
Concentrations of metals (ng 1-r) detected in seawater in Hawaii.
S. Kaneohe Bay
Element
As
Ag
Cd
Cr
cu
Hg
Ni
Pb
Se
Zn
TBT
Common sources
Pesticides
Home, photography
Rubber
Plating
Wood preservative
Health service
Plating
Batteries, gasoline
Electrical, shampoo
Rubber, plating
Anti-fouling paints
Hilo
Bay*
Keehi
Lagoon*
Kahana
Bay*
0.940
§
0.133
0.324
0.509
0.001
1.650
0.028
lI
0.560
0.890
9
0.019
0.239
1.330
0.001
0.680
0.042
n
-
1.190
§
0.021
0.528
0.430
0.001
3.390
0.056
n
19751_
_
0.007
0.032
0.012
0.003
0.003
0.003
1989*$
0.960
§
0.007
0.324
0.856
0.001
4.180
< 0.014
ll
0.210
0.195
0.006
Kaneohe
MCAS*
Pearl
Harbor*
Hawaii DOH
Limits*
0
0.001
6.150
1.400
§
0.016
0.290
2.331
0.001
2.970
0.028
!I
36.000
No standard
9.300
50.000
2.900
0.025
8.300
5.600
71.000
86.000
0.010
-
*Source: Hawaii Department of Health, Draft Report, samples collected November 1989.
$Source: Young etal. (1976).
$(TBT) Source: Naval Oceans Systems Center, J. Grovhaug, pers. comm., 1991.
$Non-detectable (< 0.001 pg 1-r).
ITNon-detectable (< 0.004 ng 1-r).
-, Not analysed.
TABLE 7
Concentrations of metals (pg g-l dry wt) in Kaneohe Bay sediments.*
Marine base sites
Element
As
Ag
Cd
Cr
CU
Hg
Ni
Pb
Common sources
1
2
3
4
5
Pesticides
Home, photography
Rubber
Plating
Wood preservative
Health service
Plating
Batteries, gasoline
4.700
0.036
t
55.000
14.000
0.038
35.000
12.000
7.100
0.028
0.120
< 0.015
0.830
co.015
4.720
co.015
17.;00
1.500
< 0.002
59.000
1.600
21.000
5.400
< 0.002
67.000
3.300
t
t
90.000
23.000
0.003
42.000
20.000
28.000
4.500
0.006
20.000
6.500
*Source: Naval Oceans Systems Center, R. S. Henderson, pers. comm., 1992.
TNon-detectable (< 0.003 ng g-l).
652
t
Volume fO/Number
lO/October
1995
1991; Goh, 1991). Some coral species may be able to
tolerate or detoxify trace metals, although growth rates
may be affected and community structures will show
responses
from
differential
species
sensitivities
(Howard & Brown, 1984; Brown & Howard, 1985).
The coral Porites futeci exhibits a bleaching response on
exposure to iron but appears to develop a tolerance
over time (Harland & Brown, 1989). In general,
although high concentrations
of toxicants have been
documented, almost nothing is known about the shortterm or long-term effects of toxic compounds on
tropical and sub-tropical marine organisms.
Despite past and current concerns about the toxicity
and persistence of various environmental contaminants
(heavy metals and pesticides),
few studies have
documented their concentrations
in tropical or subtropical marine biota. Over the past three decades,
there has been a growing trend toward a greater usage
of persistent contaminants (such as DDT and chlordane) in tropical areas with a corresponding decrease in
many temperate countries where such usage has been
banned (Greenpeace, 1992). A similar trend has been
noted for lead, for which inputs from industrialized
nations have been reduced but countered
by a
corresponding increase in Asian countries (Flegal &
Stukas, 1987). The present study shows that organic
pesticides such as chlordane and dieldrin may be
present at human health-threatening concentrations in
bivalve tissues for years after their usage has been
restricted, and suggests the need for similar screening
studies in other tropical and sub-tropical
marine
ecosystems.
The authors wish to thank P. Helfrich, M. McCartney and other
financial supporters of the Kaneohe Bay Environmental Fund, and
participants in the 1991 Kaneohe Bay Environmental Workshop. C. L.
Hunter was supported in part by the Office of Naval Research Grant
No. N00014-92-J-1852. This paper is dedicated to the memory of Dr
Carl H. Honig, whose insightful questioning encouraged the initiation
of this research. This is contribution No. 975 from the Hawaii Institute
of Marine Biology.
Acevedo, R. (1991). Preliminary observations on effects of pesticides
carbaryl, naphthol, and chlorpyrifos on planulae of the hermatypic
coral &illopora damicornis. Pac. Sci. 45; 287-289.
Avline. G. M. (19741. Uutake of cadmium, zinc. cotter, lead and
‘chrimium in‘the Tacit% Oyster, Crassostrea &gas: -grown in the
Tamar River,,Tasmania. War. Res. 8,729-738.
Brown, B. & Holley, M. C. (1982). Metal levels associated with tin
dredging and smelting and their effect upon intertidal reef flats at Ko
Phuket, Thailand. CoralReefs 1,131-137.
Brown, B. & Howard, S. (1985). Responses of coelenterates to trace
metals: a tield and laboratory evaluation. Proc. Fifth Int. Coral Reef
Gong., Vol. 6, pp. 465-470. Antenne Museum-EPHE,
Moorea,
French Polynesia.
Cajal-Medrano, R. & Gutiermz-Galindo, E. A. (1981). Concentration
et distribution du DDT dans les huitres Crassostrea gigas et Ostrea
edulis sur la core de basse California. Rev Int. Oceanogr. Med. 62,
39-45.
Campos, N. H. (1988). Selected bivalves for monitoring of heavy metal
contamination in the Colombian Caribbean. In Metals in Coastal
Environment of Latin America (U. Seeliger, L. D. Lacerda & S. R.
Patachineelarn’eds), pp. 270-275.
Cantillo. A. Y. & Lauenstein. G. G. 119921. NOAA National Status and
Trends Quality Assurance Program Intercomparison
Exercise
Results. Marine Technical Society, Symposium. October 1992,
Washington DC, 7 pp.
Chan, H. M. (1989). Temporal and spatial fluctuations in metal
concentrations in transplanted mussels in Hong Kong. Mar. Pollut.
Bull. 20.82-86.
Devaney, D. M., Kelly, M., Lee, P. J. & Motteler, L. S. (1982). Kaneohe:
A History of Change (1778-1950). B. P. Bishop Museum, Honolulu,
Hawaii.
Dougherty, G. (1988). Heavy metal concentrations in bivalves from
Fiji’s coastal waters. Mar. Pollut. Bull. 19,81-84.
Eisler, R. (1990). Chlordane hazards to fish, wildlife, and invertebrates.
US Fish Wildl. Serv Biol. Rep. 85,49.
Farrington, J. H., Goldberg, E. D., Risebrough, R. W., Martin, J. H. &
Bowen, V. T. (1983). U.S. Mussel Watch 1976-1978: an overview of
the trace1 metal, DDE, PCB, hydrocarbon and artificial radionuclide
data. Environ. Sci. Technol. 17,490-496.
Flegal, A. R. & Stukas, V J. (1987). Accuracy and precision of lead
isotopic composition measurements in sea water. Mar. Chem. 22,
163-177.
Glynn, P. W., Howard, L. S., Corcoran, E. & Freay, A. D. (1984). The
occurrence and toxicity of herbicides in reef building corals. Mar
Pollut. Bull. 15,370-374.
Glynn, P. W., Szmant, A. M., Corcoran, E. F. & Cofer-Shabica, S. V.
(1989). Condition of coral reef cnidarians from the northern Florida
reef tract: pesticides, heavy metals, and histopathological examination. Mar. Pollut. Bull. 20,568-576.
Goh, B. P. L. (1991). Mortality and settlement success of Pocillopora
damicornis planula larvae during recovery from low levels of nickel.
Pac. Sri. 45,276-286.
Goldberg, E. D., Bowen, V. T., Farrington, J. W., Harvey, G., Martin, J.
H., Parker, P. L.. Risebrough, R. W., Robertson, W., Schneider, E. &
Gamble, E. (1978). The mussel watch. Environ. Conserv 5, lOl125.
Goldberg, E. D., Koide, M., Hodge, V., Flegal, A. R. & Martin, J.
(1983). US mussel watch: 1977-78 results on trace metals and
radionuclides. Estuar Coastal Shelf Sci. 16,69-93.
Greenpeace (1992). Overview of 1991 exports of selected, banned, and
never registered pesticides. Port Import Export Exporting Service. J.
Commerce Trade Info. Service(New York) 11 February 1992.
Guzman, H. M. & Jimenez, C. E. (1992). Contamination of coral reefs
by heavy metals along the Caribbean coast of Central America
(Costa Rica and Panama). Mar Pollut. Bull. 24554-561.
Hallecher, L. E., Kho. E. B., Bernard, N. D., Orcutt. A. M., Dudley, W.
C. & Hammond, T. M. (1985). Distribution of arsenic in the
sediments and biota of Hilo Bay, Hawaii. Pac. Sci. 39,266-273.
Hanna, R. G. and Muir, G. L. (1990). Red Sea corals as biomonitors of
trace metal pollution. Environ. Monit. Assess. 14, 211-222.
Harland, A. D. & Brown, B. E. (1989). Metal tolerance in the
scleractinian coral Paorites lutea. Mar. Pollut. Bull. 20,353-357.
Hiraoka, Y. (1991). Reduction of heavy metal content in Hiroshima
Bay oysters (Crassostrea gigas) by purification. Environ. Pollut. 70,
209-217.
Howard, L. S. & Brown, B. E. (1984). Heavy metals and reef corals.
Oceanogr. Mar. Biol. Ann. Rev. 22. 195-210.
Hungspreugs, M. (1988). Heavy metals and other non-oil pollutants in
southeast Asia. Ambio 17, 178-182.
Kay, E. A. (1979). Hawaiian Marine Shells. Reef and Shore Fauna of
Hawii. Section 4: Molhtsca. Bishop Mus. Press, Honolulu, Hawaii.
Leavitt, D. F., Lancaster, B. A., Lancaster, A. S. & Capuzzo, J. M.
(1990). Changes in the biochemical composition of a subtropical
bivalve, Arca zebra, in response to contaminant gradients in
Bermuda. J. Exper. Mar. Biol. Ecol. 138,85-98.
MacLeod, W. D., Brown, D. W., Friedman, A. S., Burrows, D. G.,
Maynes, O., Pearse, R., Wigren, C. A. & Bogar, R. G. (1985).
Standard Analytical Procedures of the NOAA National Analytical
Facility, 1985-1986: Extractable Toxic Organic Compounds (2nd
Edn). Noaa Technical Memorandum NMFS F/NWC-92,121 pp.
Martin, M. & Castle, W. (1984). Petrowatch: petroleum hydrocarbons,
synthetic organic compounds, and heavy metals in mussels from the
Monterey Bay area of central California. Mar. Pollut. BUN. 15, 259266.
Martin, M. & Gutierrez-Galindo, E. (1989). Pesticides and PCBs in
oysters from Mazatlan, Sinaloa, Mexico. Mar Pollut. Bull. 20, 469472.
Menesveta, P. & Cheevaparanapiwat,
V. (1981). Heavy metals,
organochlorine pesticides and PCBs in green mussels, mullet and
sediments of river mouths in Thailand. Mar. Pollut. Bull. 12, 19-25.
Moden, J. C. (1969). Residues in fish, wildlife and estuaries. Pest.
Monit. J. 3, 1-7.
NOAA (1989). National
Status and Trends Program for Marine
Environmental Quality Progress Report: A Summary of Data on
Tissue Contamination from the First Three Years (1986-1988) of
the Mussel Watch Project. National Oceanic and Atmospheric
Administration. Tech. Memo. NOS OMA 49, NOAA/NOS/Coastal
and Estuarine Assessment Branch, Rockville, MD, 122 pp.
Okazaki. R. K. & Panietz, M. H. (1981). Depuration of twelve trace
metals in tissues of the oysters C’rassostrea gigas and C‘. \Yrginica.
Mar. Biol. 63, 113-120.
653
Marine Pollution Bulletin
Olafson, R. W. (1978). Effect of agricultural activity on levels of
organochlorine pesticides in hard corals, fish and molluscs from the
Great Barrier Reef. Mar. Environ. Res. 1,87-107.
Osibanjo, 0. & Bamgbose, 0. (1990). Chlorinated hydrocarbons in
marine fish and shellfish of Nigeria. Mar. Pollur. Bull. 21,581-586.
Paez-Osuna, F., Botello, A. V., Villanueva, S. (1986). Heavy metals in
Coatzacoalcos Estuary and Ostion Lagoon, Mexico. Mar. Pollur.
Bull. 17,516-519.
Phillips, D. J. H. (1976). The common mussel Myrilus edulis as an
indicator of pollution by zinc, cadmium, lead and copper. I. Effects
of the environmental variables on uptake of metals. Mar. Biol. 38,
59-69.
Phillips, D. J. H.
Applied Science
Phillips, D. J. H.
biomonitors in
(1980). Quantitative Aquatic Biological Indicators.
Publishers Ltd, London.
(1991). Selected trace elements and the use of
sub-tropical and tropical marine ecosystems. Ra!
Environ. Conram. Toxicol. 120,105-130.
Phillips, D. J. H. & Muttarasin, K. (1984). Trace metals in bivalve
molluscs from Thailand. Mar. Environ. Res. 15,215-234.
Phillips, D. J. H., Ho, C. T. & Ng, L. H. (1982). Trace elements in the
Pacific Oyster in Hong Kong. Arch. Environm. Conram. Toxic. 11,
533-537.
Pridmore, R. D., Roper, D. S. & Hewitt, J. E. (1990). Variation in
composition and condition of the Pacific Oyster, Crassosrrea gigas,
along a pollution gradient in Manukau Harbor, New Zealand. Mar.
Environ. Res. 30,163-177.
Pridmore, R. D., Thrush, S. F., Wilcock, R. J., Smith, T. J., Hewitt, H. E.
& Cummings, V. J. (1991). Effect of the organochlorine pesticide
technical chlordane on the population structure of suspension and
deposit feeding bivalves. Mar. Ecol. Prog. Ser. 76,261-271.
Ramesh, A., Tanabe, S., Subramanian, A. N., Mohan, D., Venugopalan,
V. K. & Tatsukawa, T. (1990). Persistent organochlorine residues in
green mussels from coastal waters of south India. Mar. Pollur. Bull.
21,587-590.
Schmitt, C. J., Ludke, J. L. & Walsh, D. F. (1981). Organochlorine
residues in fish: National Pesticide Monitoring Program, 1970-1974.
US Fish WildlifeServ. Pest. Monir. J. 14.
Schmitt, C. J., Ribick, M. A., Ludky, J. L. & May, T. W. (1983). National
Pesticide Monitoring Program Organochlorine Residues in Freshwater Fish, 1976-1979. US Fish Wildlife Service.
Smith, D. R., Stephenson, M. D. & Flegal, A. R. (1986). Trace metals in
mussels transplanted to San Francisco Bay. Environ. Toxicol.
Conram. $129-138.
Smith, S. V., Chave, K. E. & Kam, D. T. 0. (1973). Atlas of Kaneohe
654
Bay: A Reef Ecosystem Under Stress. Univ. Hawaii Sea Grant Pub.
TR-72-01.128 pp.
Smith, S. V., Kimmerer, W. J., Laws, E. A., Brock, R. E. & Walsh, T. W.
(1981). Kaneohe Bay sewage diversion experiment: perspectives on
ecosystem responses to nutritional perturbation. Pac. Sci. 35, 279395.
Soria, S. P. C. & Theede, H. (1990). Heavy metal concentrations in two
species of shellfish from Manila Bay (Philippines). In Oceunography
and Marine Pollurion: an ASEAN-EC Perspecriw (H. T. Yap, M.
Bohle-Carbonell & E. Gomez, eds), pp. 238-251. University of the
Philippines Marine Sciences Institute, Manila
State of Hawaii (1969). Evaluation of Pesticide Problems in Hawaii.
Dept. of Agriculture, Hawaii.
Stephenson, M. D., Martin, M., Lange, S. E., Flegal, A. R. & Martin, J.
H. (1979).
California Mussel Watch: 1977-1978Nol.
11: Trace metals
\
\
in the California mussel, Mytilus californianus). California State
Water Resources Control Board Water Quality Monitoring Report
No. 79-22,110 pp.
Sumner, C. E. (1978). Chlorinated hydrocarbon pesticide residues in
Pacific Oysters (Crussosrrea gigas) from Tasmania, Australia-1973.
Pest. Monir. J. 12,87-90.
Takahashi, W. (1982). Pesricide Usage Parrerns in Hawii, 1977. Pest.
Hazard Assess. Project, 92 pp. University of Hawaii, Honolulu.
Tanita, R., Johnson, J. M., Chun, M. & Maciolek, J. (1976). Organochlorine pesticides in the Hawaii Kai Marina, 1970-74. Pest. Monir.
J. 10(l), 24-29.
Thomson, J. D. (1982). Metal concentration changes in growing Pacific
Oysters, Crussosrrea gigus, cultivated in Tasmania, Australia. Mar.
Biol. 67,135-142.
Thornton, I., Watling, H. & Darracott, A. (1975). Geochemical studies
in several rivers and estuaries used for oyster rearing. Sci. Total
Environ. 4,325-336.
US Environmental Protection Agency (1993). Guidance for Assessing
Chemical Contamination Data for Use in Fish Advisories (Vol. 1:
Fish Sampling and Analysis). EPA 823-R-93-002.
US Food and Drug Administration (1975). Pesticide Analytical
Manual (Vol. 1: Methods which detect multiple residues. Section
232). US Food and Drug Administration, Rockville, MD.
Wilkinson, L. (1989). Systat: The System for Statistics. Systat Inc.,
Evanston, IL.
Young, R. H. F., Lau, L. S., Konno, S. K. & Lee, H. H. (1976). Water
Quality Monitoring: Kaneohe Bay and Selected Watersheds, July to
December 1975. Univ. Hawaii Water Res. Research Center Tech.
Rep. 98.84 pp.