Marine Environmental Research. Vol. 44, No. 3, pp. 243-262,
PII:
SOl41-1136(97)00003-Z
1997
Q 1997 Elsevier Science Ltd
All rights reserved. Printed in Great Britain
0141-1136/97 $17.00+0.00
ELSEVIER
Spatial and Temporal Variation of Selenium Concentration
in Five Species of Intertidal Molluscs
from Jervis Bay, Australia
S. Baldwin and W. Maher
Applied Science, University of Canberra, PO Box 1, Belconnen, ACT 2616, Australia
(Received 14 April 1996; revised version received 6 December 1996; accepted 29 December 1996;
published July 1997)
ABSTRACT
Spatial, temporal, intraspecies and interspecies variation of selenium concentration
inJive species of intertidal molluscs from Jervis Bay, Australia was investigated.
The selenium concentrations measured in molluscs were lower than in those
reported from overseas studies. The selenium concentrations did not d@er from
those reported for other relatively unpolluted Australian marine environments.
Nerita atramentosa had the lowest selenium concentration, followed by A.
constricta and B. nanum, then 0. angasi, with M. marginalba having the highest
concentrations of selenium. Species dtferences in selenium concentration were also
rejected in total body burdens of selenium. The dtflerences in selenium concentration among species varied temporally, with the magnitude of the dtrerences varying among months. The population distributions of selenium concentration generally
exhibited positive skewness, with most individuals within each species containing
low concentrations of selenium. Only a few individuals exhibited high concentrations of selenium, extending the right tail of the frequency distribution. Skewness
could not be explained by mass and size differences and is probably the result of
micro-habitat dtj-erences. Selenium concentrations did not have any consistent
relationship with mass or length of the species. The trend was towards lower
selenium concentrations as mass of the mollusc increased. This means that mass
or length cannot be used as an index of selenium concentrations in populations of
the species examined in this study. Significant variation in selenium concentration
existed on all spatial scales (location, site) for all species with the exception of
the bivalve 0. angasi. For the gastropods, the order of sites from lowest to highest
selenium concentration d@ers among sampling times, with no predominance of one
site over another. All species showed signtficant temporal variation in selenium
concentration and selenium body burdens but there were no consistent trends over
time, or consistent relationships with body mass. At most sites the lowest selenium
concentrations and selenium body burdens were recorded in January and associated with high body tissue mass in 0. angasi, and spawning in N. atramentosa,
B. Nanum and M. marginalba. 0 1997 Elsevier Science Ltd
243
244
S. Baldwin.
W. Muhrr
INTRODUCTION
Selenium is of interest because it is classified as both an essential element for animals
(Schwartz and Faltz, 1957) and is toxic at elevated levels (Moxon and Olsen, 1974;
Ganther,
1974). Sub-lethal effects such as edema, tissue degeneration
and chromosomal
abberations
are also prevalent in animals exposed to high concentrations
of selenium from
natural or human induced sources (Sorensen rt al., 1984, Sorensen and Baver, 1983.
Gillespie and Baumann,
1986).
Maher rt al. (1992) and Maher and Batley (1990) reviewed current literature on selenium in Australian
marine organisms
and suggested that future Australian
research
should be directed toward accumulating
information
about:
1. selenium content of waters. sediment and biota of nearshore
2. speciation of selenium in water sediments and biota; and
3. selenium’s relationship
with other trace elements.
environments:
Their concern was that selenium has not been characterized
enough in Australian
ecosystems to know if it poses an environmental
hazard.
The first research directive forms the basis of this study. The habitat chosen for study
was the intertidal rocky shore of Jervis Bay, Australia which supports more than 51 species of flora and fauna (Jervis Bay Baseline Studies, 1990). Underwood
and Atkinson
(1995) proposed that one future disturbance
affecting rocky shore habitats in Jervis Bay
(and elsewhere) may stem from water-borne
chemicals from urban and industrial sewage,
effluents, and run-off. The responses of Australian
marine organisms
to chemicals are
largely unknown,
stressing the need to study and strengthen our current knowledge base
of the occurrence of trace metals in organisms.
The use of organisms as biomonitors
of metal concentrations
in marine and estuarine
environments
has been summarized by Phillips (1977, 1980, 1990). Contamination
is often
geographically
patchy because of factors such as wind direction,
storm events, intermittent chemical inputs from point and non-point
sources, and localized differences in
sediment types. Analysis of grab samples of water only gives a snapshot of information
at
that one time, and this information
is difficult to relate to effects on the biological components of the environment.
Organisms are able to integrate the relative concentrations
and bioavailability
of metals over their particular
spatial and temporal ranges, and so
provide a measure of potential
ecological
and human health risks (McCarthy
and
Shugart, 1990).
Prior to using organisms as biomonitors,
Gorden et ul. (1980) stated that an estimate of
trace metal and other pollutant variability must be established to subsequently
achieve the
objectives of baseline or monitoring
studies. If element concentration
variation
is not
characterized,
then differences
in environmental
pollutant
concentrations
caused by
anthropogenic
activity may be uninterpretable.
There is a paucity of information
regarding selenium in Australian
marine environments to adequately account for any natural variation existing in the biota (Maher and
Batley, 1990). Variations may exist because of spatial (location, site) differences, temporal
(time or season) differences, or species differences.
The objectives of this study were to measure the selenium concentrations
in five intertidal mollusc species commonly
found on the rocky intertidal
shores of Jervis Bay to
determine the:
Spatial and temporal variation of selenium concentration
245
0 interspecies variation in selenium concentration
frequency distribution of selenium concentrations in populations and thus ‘inherent’
variability
l effect of mass and length on selenium concentrations
l spatial selenium concentration
variability
l temporal
selenium concentration and total selenium body burden variability in
relationship to mass variation.
l
SELECTION
OF SITES AND STUDY DESIGN
Study area
Jervis Bay lies on the south coast of New South Wales some 180 km south of Sydney. Sites
relevant to this study are shown in Fig. 1.
The geology of the area is predominantly sandstone overlain by varying depths of
deposited sand (Taylor et al., 1995). Three freshwater inflows drain into Jervis Bay:
Moona Moona Creek and Currumbene Creek draining the western land of the bay and
Carama inlet in the north (Fig. 1). Total catchment of the bay is 400 km2, a small area
when compared to the water area of Jervis Bay at 102 km2. The waterways support mangrove and saltmarsh communities which, in association with the sandy soils of the catchment, filter the water inflows of silt and particulates. This, along with the absence of large
inflows draining into the bay, results in Jervis Bay having clear waters (Jones et al., 1995;
Taylor et al., 1995).
Holloway et al. (1992) surveyed the temperature and salinity profiles of the Jervis Bay
region from May 1990 to December 1991. Salinity shows little annual variation in the bay
and tends to be relatively constant at 35.4%, although salinities as high as 35.55% were
measured between April and May 1991, and as low as 34.9% in July 1991. The latter
reading corresponded to a period of heavy rainfall and river discharge into the bay. Water
temperature varies between 15 “C in August-September and 23 “C in January.
Study sites
Three rocky shore intertidal locations were sampled around Jervis Bay (Fig. 1). Two sites
(5 mx5 m plots) were randomly selected at each location, and these sites were sampled
during subsequent sampling runs.
Plantation
Point
Plantation Point is a flat mudstone platform about 200m long and 1OOmwide. A sewage
outfall pipe discharges tertiary treated sewage due east from this location. Site 1 (PLSl) is
on the southern end of the platform and site 2 (PLS2) is on the northern end of the platform. The sewage pipe lies between the two sites.
Blenheim
Beach
The rocky outcrop on the northern end of the beach was sampled with site 1 (BLSl) on
the southern tip of the platform, and site 2 (BLS2) about 1OOmfarther north. Site 2 is
more exposed to wave energy than site 1.
S. Baldwin.
246
W. Maher
Fig. 1. Location of sampling sites.
Bristol
Point
Bristol Point is a sandstone rock platform about 200 m long and 30 m wide. Site 1 (BRSl)
is on the eastern extreme of the platform and site 2 (BRSZ) about 150 m away on the
western end of the platform.
Organism selection
Five mollusc
species were sampled
cium
Nerita
nanum,
utrummtosu,
in this study. Three were grazing gastropods;
Bembiand Austrocochleu
constricta;
one was a filter-feeding
241
Spatial and temporal variation of selenium concentration
bivalve, Ostrea angasi; and one was a carnivorous gastropod, Morula marginalba. These
species are representative of molluscs found along the eastern Australian coast from
Queensland in the north to Tasmania in the south (Underwood, 1974; Dakin, 1988). All
these organisms occur in the mid-littoral zone (Underwood, 1974).
Sampling design
A nested sampling design (Fig. 2) was used to the assess the relative contribution of each
factor (time, species, location and site) to the total variation in selenium concentration.
Sampling was conducted monthly from October 1990 to September 1991. Only samples
from six of the twelve months sampled were selected to be analyzed for selenium because of
analysis constraints. The months were chosen to assess summer, autumn, winter and spring
seasonal variations. The level of replication within each month was not sufficient to characterize seasonal variations so only temporal differences were analyzed. Larger sample sizes
were collected in January to examine the effects of mass and length on selenium concentration.
SAMPLE PREPARATION
Processing and storage
Molluscs and algae were rinsed with deionised water to remove epiphytic growths and
particulates from the surfaces of the samples, depurated in clean water for 12 hr and then
Replicates
Factors
Month
1,; 2
;
Location
A
Samples*
1
A
2
3
4
5
*In Month l(January) 15 samples were collected for analysis
Fig. 2.
Sampling design.
A
248
S. Bullwin. W. Maher
frozen until returned to the laboratory.
After defrosting at room temperature,
oysters
were shucked from their shells while the shells of the gastropod molluscs were cracked
with a hammer and soft tissues removed using plastic forceps to extract stubborn muscle
tissue adhering to the columellar
of the shell. All tissues were placed into acid-washed
20ml plastic-capped
viais and frozen until digested.
Sample digestion and analysis
Samples were freeze-dried and digested with nitric acid using a low volume microwave
digestion procedure (Baldwin et al.. 1994). Selenium was determined
by electrothermal
atomic absorption
spectroscopy,
using palladium and magnesium
as the matrix modifier
(Deaker and Maher, 1995). The accuracy of the procedure has been previously assessed
by the analysis of a range of standard reference materials (Deaker and Maher, 1995). In
this study, reference materials NIST 1966a (Oyster tissue) and NRCC Dorm 1 (Dogfish
muscle) were routinely run with each sample batch digested. Recoveries for selenium of
2.2 * 0.2pg g -’ and 1.54 i 0.08 I-(g g -’ dry mass. respectively, were in agreement with the
certified values (2.08 f 0.2 pg g- ’ and 1.62 i 0.12 pug g ’ dry mass).
RESULTS
Interspecies variation of selenium concentration
Selenium concentration
(pg g ’ dry mass). dry mass and length of shell in the five mollusc
species studied over six sampling times were characterized
using descriptive statistics of
the data pooled across the six sites (Table 1).
Shell material of each of the mollusc species from the January run were also digested.
Five random samples of shells of each species were analyzed for selenium as a pilot study
to determine
selenium concentration
ranges. Selenium was not present in quantifiable
concentrations
(0.03 pg Se gg’ dry mass) in any of the shell material analyzed. so no further measurements
of shell selenium concentration
were performed.
N. atramentosa
nearly always had the lowest selenium concentrations,
followed by
A. constricta or B. nanum then 0. angasi, with M. marginalba having the highest concentrations of selenium (Table 1, Fig. 3).
Mass and length were not significantly
correlated @>0.05) in these organisms. There
were consistent trends in mean mass between species at each sampling time (Table 1).
N. atramentosa had the largest masses followed usually by 0. angasi or A. constricta, then
M. marginalha, and B. nanum. Similarly. there were consistent
trends in relative shell
lengths between species regardless of sampling time (Table I), but these were often not in
the same order as the mass trends. 0. angasi had the greatest mean shell length followed
by M. marginalba and N. atramentosa, B. nanum and A. constricta.
Frequency distribution of selenium in organisms
The distributions
of selenium concentration
in populations
were rarely normal (see normality, kurtosis and skewness columns in Table 1). Figure 3 shows the frequency histograms of selenium concentration
in each mollusc species for January pooled data which
graphically presents the pronounced
positive skew found for most populations.
SE = Standard
0. angasi
M. marginalba
A. constricta
N. atramentosa
B. nanum
Species
30
95
30
30
30
30
30
82
30
30
30
30
30
82
30
30
30
30
30
88
30
30
30
30
15
29
15
15
15
15
1.390
4.622
0.922
2.890
2.860
3.240
3.750
1.520
0.730
1.180
I .830
0.990
1.350
1.450
0.457
0.451
0.928
0.831
0.546
0.608
0.046
0.148
0.054
0.164
0.184
0.056
1.490
0.331
0.893
1.230
Mean
Statistics
_
62.7
93.4
177.5
54. I
87.2
87.0
31.5
101.5
190.9
94.4
217.5
91.9
46. I
71.5
66.0
56.3
53.9
53.2
83.1
96.4
69.8
61.1
74.4
85.9
33.7
63.7
78.2
38.4
37.8
38.3
of variation;
0.090
0.002
0.020
0.020
0.060
0.030
0.010
0.190
0.030
0.110
0.130
0.140
0.130
0.700
0.090
0.370
0.320
0.440
0.590
0.130
0.070
0.240
0.180
0.090
0.130
0.090
0.050
0.040
0.300
0.080
N = Sample
0.410
0.330
0.510
0.720
0.480
0.540
0.045
0.098
0.018
0.230
0.155
0.025
1.470
0.300
0.810
1.010
1.410
1.450
3.570
0.630
2.390
2.540
2.300
2.850
1.310
0.730
0.950
1.700
0.960
1.570
Range
size; W = Shapiro-Wilks
0.08
2.54
19.00
5.19
-1.33
-0.49
1.56
3.46
15.18
6.41
2.83
0.55
12.14
xl.45
-0.05
-1.27
3.58
a.69
0.43
1.61
0.14
0.35
1.48
0.59
0.16
30.67
1.34
-0.99
1.78
4.25
(VI)
Kurtosis
TABLE 1
for Five Mollusc
0.05-I .09
0.02-2.12
0.07-8.8
O.l9%2.45
0.02-2. I6
0.03%1.91
O.OlXl.08
0.01-0.76
0.01-4.52
0.015-1.37
0.02-0.74
0.02-0.19
0.05-5.99
0.02-I .09
0.0&2.15
0.01&2.53
0.074.12
0.01-2.86
0.5614.06
0.02-3.94
0.42-8.34
0.37-7.65
0.2&10.47
0.18-15.43
0.89-2.69
0.03-1.58
0.1&3.32
0.562.99
0.44-1.95
0.28-I .81
(all Sites Pooled)
Selenium (pg g-’ dry mass)
c. v. Median
SE+/-
error of mean; CV = Coefficient
4
6
8
9
I
4
6
8
9
12
I
4
6
8
9
12
1
4
6
8
9
12
1
4
6
8
9
12
I
12
Month N
Descriptive
statistic
3.68
2.67
1.71
I .29
2.75
0.58
0.58
0.21
1.20
a.05
1.14
1.41
0.88
0.65
1.32
0.87
0.88
5.48
3.18
a).04
0.93
-1.07
0.0806
0.0001
0.0001
0.0003
0.0001
0.0095
0.0008
0.0001
0.0001
0.0001
0.0001
0.000 I
NS
0.000 I
NS
S-NS
0.0356
NS
0.0007
0.0001
0.0156
NS
0.00 I5
0.0001
NS
NS
0.0195
NS
NS
0.0066
pv4
Normalitv
for normality.
1.88
0.05
I.43
4.17
1.92
a.17
0.63
0.04
fg1l
Skewness
Species at Six Sampling
0.107
0.064
0.058
0.093
0.086
0.066
0.230
0.222
0.214
0.245
0.301
0.263
0.107
0.163
0.132
0.131
0.140
0.155
0.108
0.092
0.089
0.138
0.103
0.086
0.086
0.145
0.094
0.107
0.180
0.192
0.006
0.002
0.005
0.006
0.006
0.003
0.020
0.010
0.010
0.020
0.030
0.020
0.030
0.010
0.010
0.010
0.010
0.010
0.010
0.010
0.010
0.030
0.010
0.010
0.020
0.040
0.010
1.010
0.020
0.010
Dry Mass (g)
SE+/Mean
Times
16.70
14.36
14.73
15.97
15.57
15.63
20.30
18.70
18.90
18.40
18.90
18.90
15.27
18.50
16.73
17.00
15.90
16.70
19.23
19.00
20.00
18.87
20.67
20.03
29.67
31.60
26.20
34.13
34.67
31.80
Length
Mean
0.25
0.17
0.39
0.034
0.30
0.31
0.58
0.27
0.33
0.36
0.76
0.41
0.33
1.26
0.32
0.29
0.21
0.17
0.39
0.32
0.53
0.46
0.63
0.71
1.05
I .06
1.69
2.67
1.03
1.17
(mm)
SE+/-
250
[al
PI
6
k
,
’
2
:
I
i
Ml
I
I
L
Fig. 3. Frequency
histograms
of selenium concentration
in five intertidal molluscs species
B. namum, (b) N. utrarnentnsa, (c) A. constrictu. (d) M. marginal&. (e) 0. angasi.
(a)
Spatial and temporal variationof selenium concentration
251
The distribution of selenium concentrations in B. nanum approaches normality only in
December (Table l), with kurtosis and skewness values of 0.08 and 0.05, respectively. The
Shapiro-Wilks (W) statistic provides further support that the selenium concentrations
exhibit normal distribution for B. nanum in December. The distribution of selenium in N.
atramentosa was symmetrical only in the December (Table l), but exhibits leptokurtic
distributions at each sampling time, resulting in non-normal selenium concentration distributions throughout the population. Sampling times other than December produced
positively skewed distributions (Table 1). Selenium distribution in A. constricta was normal in December, April and September, whereas selenium distribution in June was very
close to normality (Table 1). Selenium distributions for this species vary between leptokurtic and platykurtic for the remaining sampling times, but are positively skewed. Selenium distributions in M. marginalba populations were always slightly positively skewed
and generally leptokurtic, except in June when the distribution was found to be normal
based on the W statistic (Table 1). 0. angasi showed normal distributions of selenium
concentration in December, January, June and August (Table 1). In April, the distribution was positively skewed and leptokurtic. In September, the distribution was negatively
skewed and slightly platykurtic.
Effects of mass and length on selenium concentration
Figure 4 shows scatterplots of selenium concentration and dry mass for each species in
January. The trend was towards lower selenium concentrations as the mass of the mollusc
increased. B. nanum showed a significant regression for the pooled data (Fig. 4). Only two
of the sites BRS2 (r* = 0.39,~ < 0.05) and PLSl (r* = 0.61,~ < 0.001) had significant
relationships between mass and selenium concentration. It was observed that individual
samples of less than 0.05 g dry mass had higher selenium concentrations. N. atramentosa
showed little relationship between mass and selenium concentration when data was
pooled across the sites (Fig. 4). At individual sites no significant relationships between
mass and selenium concentration were found. A. constricta had a significant regression
value for pooled data (Fig. 4). On a site basis, only PLS2 had a significant relationship
between mass and selenium concentration (r* = 0.42,~ < 0.05). Mass was therefore not a
dominant factor influencing selenium concentration at individual sites. M. marginalba
showed no significant relationship between selenium concentration and mass when the
data was pooled (Fig. 4). Only one site (BRSZ) had a significant relationship between
mass and selenium concentration (r2 = 0.4,~ -C0.05). It was again observed that individual samples of less than 0.05grams dry mass had higher selenium concentrations. The
pooled data for 0. angasi (Fig. 4) showed no relationship between mass and selenium
concentration (r* = 0.564,~ > 0.05). Only one site, PLSl, had a significant relationship
between mass and selenium concentration (r* = 0.81,~ < 0.001).
Length as a variable did not influence selenium concentration as no significant correlations
of selenium concentration and length were found for pooled data or individual site data.
Spatial and temporal variability
Nested analysis of variance
The possible sources that could contribute to selenium concentration variability, identified
at the outset of the study, were species, time, location and site. Gender has not been found
252
S. Baldwin.
7.
T
.
1.6
W. Maher
r=.o.s,
..*
Fig. 4. Scatterplots
of selenium concentration
versus dry mass for five intertidal molluscs species
(a) B. namum, (b) N. atramentosa, (c) A. constricta, (d) M. marginalba, (e) 0. ungasi.
Spatial and temporal variationof selenium concentration
253
to cause differences in selenium concentration (Maher, unpublished data). The factor ‘site’
was nested in location because two sites were selected within three locations (Fig. 2). A
four-way analysis of Variance (ANOVA) showed significantly different selenium concentrations in organisms among locations, between times, among species and among sites. A
non-significant result for interaction between location and time indicated that the order of
selenium concentration differences between locations was the same at each sampling time.
Significant three-way interactions between Location*Time*Species and Time*Species*Site
(Location) were found, implying that variations in selenium concentrations at location
and site spatial scales were in differing orders and possibly varying magnitudes for species
throughout time, i.e. no consistent trend in differences of selenium concentration was
apparent for these factors.
To further determine intraspecies spatial and temporal variability the data was sorted
by species, and a series of three-way nested ANOVAs [Time, Location, Site (Location)]
were run. All the factors and interactions analysed were significant sources of variability
of selenium concentration in B. nanum and N. atramentosa. For A. constricta location
and the interaction between Time and Site (Location) were significant sources of variability of selenium concentration. For M. marginafba the Site (Location) and Locations
interaction with Time were not significant sources of selenium concentration variation.
For O.angasi only Time was identified as a significant source of variation in selenium
concentration.
Spatial selenium concentration variation at each sampling time
Analysis of variance using two-way ANOVAs [Location, Site (Location)], showed that
significant variation in selenium concentration exists on all spatial scales (Location, Site)
for all species, with the exception of 0. angasi. Spatial differences in selenium concentration of 0. angasi at Location and Site scales were only detected in December, where selenium concentrations measured at PLSl were significantly different to the other two sites,
PLS2 and BRSl (Table 2). For the gastropods, the order of sites from smallest to greatest
selenium concentration often differed among sampling times (Table 2) with no apparent
predominance of one site over another.
Temporal variation
All the species investigated in this study showed significant temporal variation in mean
selenium concentration (Fig. 5). In January the lowest selenium concentrations were
recorded in A. constricta, M. marginalba and 0. angasi for almost all sites. Highest
selenium concentrations
occurred in cooler seasons i.e. April through to August
(Fig. 5).
Selenium concentration and selenium body burdens were not significantly correlated
(r2 = 0.079 - 0.718, p < 0.005) with changes in mass in B. namum, N. atrametosa, A.
constricta and M. marginalba. Average masses are uniform through time for all these
molluscs (Figs 5ad). Temporal variation in total selenium body burdens follow the same
trends as the selenium concentrations (Figs 5ad) indicating that selenium was taken up
and lost over time. A pronounced loss of selenium occurs in January for all molluscs
except N. atramentosa. For 0. angasi, selenium concentration was negatively correlated
with mass (r2 = 0.40 1, p < 0.00 1). The temporal variation of selenium body burden in
0. angasi (Fig. 5e) indicated that selenium was accumulated during cooler seasons (AprilSeptember) and lost during summer.
254
S. Baldwin, W. Maher
TABLE 2
Species Selenium Concentration
Differences for each Sampling Time. I = PLSl, 2 = PLS2, 3 = BLSl.
4 = BLS2, 5 = BRS 1, 6 = BRS2; Sites are Arranged in Ascending Selenium Concentration
with Sites
not Significantly Different (p < 0.05) from each other Underlined.
Species
B. nanum
N. atramentosa
A. constricta
Site
df Pr> F/HSD
df’ Pr > F/HSD
December
29
0.0001
165432
29
0.05
521436
January
89
0.018
243615
89
0.05
24653
df‘ Pr > F!HSD
M. marginalba
0. angasi
_
_~~
df Pr> F/HSD df’ Pr> F,‘HSD
- 29
0.005
_i~4561
29
0.05
21 5364
29
0.0007
521
89
0.0015
‘16453
89
0.0029
516342
29
0.05
125
29
0.05
I25
29
0.05
125
0.05
2 I 5
I
April
29
0.0036
263145
29
0.05
562314
29
0.05
523641
29
0.0093
251634
June
29
0.0095
142356
29
0.05
3_5_42_3_6
29
0.05
261534
29
0.05
26453
I
August
29
0.0001
156423
29
0.05
516423
29
0.05
456213
29
0.05
142653
29
September
29
0.0001
462153
29
0.005 I
‘43561
29
0.005 1
245613
29
0.0006
241653
29
Pr > F denotes probability of difference occuring HSD is the order attained
underlined values not significantly different 0, < 0.05) from one another.
0.05
251
_~
by Turkey’s test with
DISCUSSION
Interspecies variation of selenium concentration
The mean selenium concentrations
measured in this study for herbivorous
gastropods
(0.05-l .5 1_~gSe/g dry mass), for filter feeding bivalves (0.7-l .8 PLLg
Se/g dry mass) and for
carnivorous
gastropods (0.94.6 pg Se/g dry mass) were lower than those reported in other
studies of relatively unpolluted
environments;
for bivalves they range between 1.3 and
11 pg Se/g dry mass (Okazaki and Panietz. 198 I : Lobe1 et ul., 199 I ; Lui et al.. 1987) and for
gastropods between 0.22 and 9 pg Se/g dry mass (Lui et a/., 1987). The selenium concentrations in molluscs from Jervis Bay analyzed in this study did not differ from selenium
concentrations
(0.07-2.7p.g
Se/g dry mass) measured in molluscs sampled from other
relatively unpolluted
marine environments
in Australia (Maher and Batley, 1990; Maher
et al., 1992).
Two possible hypotheses may explain these findings. Australian
marine biota do not
accumulate
selenium to the same extent as species studied elsewhere or natural concentrations of selenium are lower in Australian
rocks, soils and water than in overseas
environments
There has not been enough research into Australian
marine species’ and
their ability to accumulate selenium to yet justify the first supposition.
Laboratory
uptake
experiments are required to quantify each species ability to accumulate selenium under a
range of control conditions.
The second hypothesis is highly likely as Australian
soils are
selenium deficient (Berrow and Ure. 1989).
The results show that the three grazing species tended to have the lowest selenium
concentrations,
while the omnivorous
filter-feeder
and carnivorous
species tended to
Spatial and temporal variation of selenium concentration
Lagmld:
. Dry Mua (#) mrotal s.lmtum
(rg)
.sdmhnn
c-
255
bL#g)
4
0.3
0.25
1.4
4.2
T
[bl
0.35 T
T 0.25
0.3
0.25
0.2
0.15
0.1
~1
0.05
0
I
_._
0.25
0.2
0.15
0.1
1.05
7
.-
-3
f*
-
- '\;*.*..
1.
'
=. :
",+.~
**
'
-
-
I
-
t:"
P
z
%
%
Fig. 5. Temporal variation of dry mass, total selenium body burden and selenium concentration
(a) B. namum, (b) N. atramentosa, (c) A. constricta, (d) M. marginalba, (e) 0. angasi.
256
S. Baldwin. W. Mahrr
contain the highest selenium concentrations.
This suggests that feeding strategies influenced
the uptake rates of selenium among the species. Underwood
(1974) has shown there are
differences in the rate of feeding between grazing species. Underwood
(1984) suggests that
there are differences in the type of food ingested by these species as well as differences in
digestion and feeding mechanisms.
Such variations in food, metabolism
and mechanical
feeding strategies have been postulated to affect the uptake and retention of trace elements
within and between species (Cossa rt al.. 1980). Another explanation
would be different
metabolic requirements
for selenium between the species, as suggested by Ireland and
Wootton
(1977) for zinc. As selenium concentration
in organisms is a product of net
uptake minus net elimination.
ie. net retention (Fowler and Benayoun,
1976; Wrench.
1979) interspecies differences in retention and elimination
mechanisms
may also cause
differences in selenium concentration.
Frequency distribution
Most of the individuals within each species contained low concentrations
of selenium, with
only a few individuals exhibiting high concentrations
extending the right tail of the frequency
distribution
(Fig. 3). Skewness cannot be explained as a size effect, as selenium concentration was not correlated to mass or length. Variability was not due to gender differences
(Marino and Enzo, 1983) as selenium concentration
differences between males and females
are small for intertidal gastropods and bivalves (Maher, unpublished
results). Lobe1 et al.
(1982,1992) and Lobe1 and Wright (1983) analyzed a number of aquatic organisms for trace
elements and also found that all the trace elements measured showed positively skewed
frequency distributions
in unpolluted
environments.
It was suggested that such inherent
variability may be the result of genetic differences in uptake processes and/or excretion rates.
Effects of mass and length on selenium concentration
Where relationships
between selenium concentration
and mass were found, the trend was
towards lower selenium concentrations
as the mass of the mollusc increased (Fig. 4). The
pattern also seems to hold even when the results were not statistically
significant. The
trend of decreasing selenium concentration
with increasing mass has been found by other
authors (Abdel-Moati
and Atta, 1991; Johns et u/., 1988; Lytle and Lytle, 1982; Cossa et
al.. 1979, 1980; Lobe1 et al., 1991). They attributed
this to the higher metabolic rates of
smaller/younger
organisms.
The decrease in trace metal concentration
in molluscs with the increase of body mass is
widely reported in the literature and appears to be a general phenomenum
in molluscs
(Boyden, 1977; Mackay et al., 1975; Cossa et ul., 1980; Lobe1 and Wright, 1982; Thomson,
1982; Phelps et al., 1985; Savari et uf., 1991; Cheung and Wong, 1992).
Johns et al. (1988) suggest age or growth may influence selenium concentrations.
Their
work on Macoma balthica (clam) revealed that only one of four study sites showed evidence
of mass influencing selenium concentrations.
Specimens collected at one site were younger
organisms than those collected at other sites, even though the range of sizes from each site
was similar. The time of exposure (age) to selenium may have influenced selenium concentrations, rather than mass. Counting growth rings in the clam gave an indication
of relative ages for the samples collected in the study of Johns et al. (ibid.). The species collected
from Jervis Bay do not exhibit identifiable growth rings, and so no age assessment could
Spatial and temporal variation of selenium concentration
251
be undertaken. Mass and length were the only approximations available to assess an
organism’s age and, as shown by Johns et al. (ibid), such morphological measurements are
not reliable predictors of age.
Spatial variability
For B. nanum, N. atramentosa, A. constricta and M. marginalba the results from this study
show that there were significant differences in selenium concentration within a species
among locations and among sites (Table 2). For 0. angasi there was no difference in
selenium concentration within a species among locations and among sites (Table 2).
The sewage outfall situated at Plantation Point (Fig. 1) was considered to be a potential
source of selenium input into Jervis Bay that might have influenced spatial differences in
selenium concentration found in biota. The sewage outfall does not appear to be a major
source of selenium as biota from the two Plantation Point sites (Table 1) did not consistently differ in selenium concentrations from those from other sites.
Examples of natural spatial variability in trace element concentrations can be found
throughout the literature (Bryan, 1973; Karbe et al., 1977; Gorden et al., 1980; Lobe1 et
al., 1982; Lobe1 and Wright, 1983; Lobel, 1987). Whole soft tissue concentrations of trace
metals have been found to differ significantly within and between sites even when studies
have been designed to eliminate physiological and ecological factors (gender, size, habitat)
which might cause differences in trace metal concentrations. Unexplained residual variability, or inherent variability, appears to be a ‘universal characteristic’ of trace metal
concentration distributions in molluscs.
The factors known to affect the accumulation and retention of elements in marine
organisms are both extrinsic (pH, salinity, temperature and chemical speciation) and
intrinsic (gender, size, diet and age) to the organism. pH and salinity in Jervis Bay are
relatively uniform through space and time, but temperature (of water and air) does change
seasonally (Holloway et al., 1992). The species analyzed in this study were subject to
habitat heterogeneity. The sampling sites, although all classed as rocky-shore habitats,
were made up of micro-habitats that included rock pools, flat rock platforms with varying
slopes, crevices and overhangs. These variations in ecological habitat create differences in
wave energy impacts, shelter, recruitment, and food availability (Fletcher, 1987; Fairweather and Underwood, 1983; Fairweather et al., 1984; Underwood and Atkinson,
1995). The subsequent biological effects may be differences in size, age and metabolism of
organisms, hence variations in selenium concentrations, even within the same species.
Growth rate has been shown to be important in determining the accumulation of selenium
(Cain et al., 1987) and other trace elements (Cossa et al., 1980; Strong and Luoma, 1981).
Growth rates of N. atramentosa vary depending on their vertical position on rocky shore
platforms (Underwood, 1984) because of the availability of algae found at different shore
heights. Molluscs on lower positions of the rocky shore have longer immersion times, hence
longer feeding times, and lower positions on rocky platforms have more moisture encouraging greater algal growth. Growth rates for B. nanum show a similar trend. Growth
correlates with algae supply and appears to be dependent on shore height. Rates of feeding between individuals of different sizes do not differ significantly (Underwood, 1984).
M. marginalba are known to sit on prey through several high and low tide periods, and
thus are exposed for part of their feeding time to heat and desiccation stress (Moran,
1985). Such stress may cause M. marginalba to cease feeding and seek shelter, which
258
S. BuMwin. W. Maher
amounts
to another factor causing variation
in food intake between individuals,
and
hence growth and selenium intake. Differences in shelter availability
on a micro-scale
between sites may enable M. marginalha to feed more at some sites, but not at others. The
two sites at Plantation
Point (PLSI and PLS2) were situated on a flat basalt rock platform
with shallow sheet depressions formed from erosion. The sites at Blenheim Beach (BLSl
and BLS2) and Bristol Point (BRSI and BRS2) were sandstone rocky outcrops with much
more slope and elevation than Plantation
Point. and deeper, more numerous rock pools.
The need for shelter from desiccation would depend on the solar radiation, so the feeding
patterns will vary over time, especially at exposed sites (PLSl and PLS2). This outcome at
exposed sites could be counteracted
by the occurrence of other sheltering factors, such as
growth of macroalgae shading the open spaces within rockpools. It was noted that in late
summer the macroalga Homosira hanksii was abundant,
especially across sites at Plantation Point (PLS) and Bristol Point (BRS).
Not only does M. marginalba exhibit irregularity in feeding patterns, but also variability
of prey species eaten (Fairweather
and Underwood,
1991) which may lead to differences
in the amounts of selenium ingested. Fairweather and Underwood (1991) have shown that
different prey species, including N. atramentosa, eggs of N. atramentosa, B. nanum, and A.
constricta, are eaten in different amounts depending on site. Reasons for this may include
prey availability,
relative sizes of prey species, or location of prey species relative to shelter
access on the shore (Fairweather
and Underwood.
1991). All the prey species were found
at each site, consequently
dietary differences may influence growth and selenium uptake
and cause selenium concentration
variation in hf. marginalba.
Gender may be a factor contributing
to site variation of selenium concentration
within
a species, depending
on the ratio of females and males collected (Lobe1 ct a/., 1991).
Measurements
of selenium concentrations
in B. tzanum and A. constricta from other Australian locations have shown no significant difference in selenium concentration
between
males and females collected at the same time (Maher, unpublished
data) and differences
due to gender are not considered to be a factor causing selenium concentration
variability
in the results presented here.
TEMPORAL
VARIABILITY
Selenium concentrations
were found to vary temporally
in this study (Fig. 5). Similar
findings that selenium and other trace elements vary on a temporal
basis have been
reported in the literature (Karbe et al., 1977; Bryan, 1973; Gault et al., 1983; Savari et al.,
1991; Lobe1 et al., 1991). As found in other studies. concentrations
of metals were highest
when algal productivity
was relatively low in the autumn and winter months while concentrations
of metals were smallest in the spring and summer months when food availability was high. In other studies of bivalve molluscs, decreases in selenium concentration
were correlated with increases in the mass of the organism (Simpson,
1979). 0. angasi
followed this pattern (Fig. 5e). The gastropods
did not show this trend as masses were
relatively constant throughout
the year (Figs 5a-d). Algal productivity
is still high in Jervis Bay, even in winter months, and the ongoing food availability results in the maintaince
of body mass of molluscs during the winter.
Phillips (1980) identified three factors which may contribute
to temporal changes in
tissue trace metal concentrations.
These were variation
in pollutant
delivery to the
Spatial and temporal variation of selenium concentration
259
environment; changes in ambient factors affecting metabolism, such as salinity and
temperature; and the organisms’ physiology, especially aspects relating to reproductive
cycles.
The mollusc species from Jervis Bay are probably not affected by variations in selenium
input into the Bay. The Jervis Bay catchment has urban areas around the bay, but no
industrial inputs. Selenium input into Jervis Bay probably does not vary temporally
because there is an absence of discharge from large sources, ie. industrial inputs, power
plants. The catchment area is small compared to the volume of water in the bay, so
freshwater inflow is comparatively small and run-off from stormwater probably does not
affect concentrations of selenium in Jervis Bay waters. Also biota from the two Plantation
Point sites near the sewage outflow did not differ in selenium concentrations from those
from other sites (see Table l), indicating that this potential point source of selenium is not
influencing selenium concentrations.
Changes in salinity can influence the uptake of trace elements (Phelps et al., 1985;
Wilson and Elkam, 1992), but the salinity in Jervis Bay does not substantially alter
through time (Holloway et af., 1992). Water temperature measurements by Holloway et
al. (1993) showed an 8 “C decrease from January to August. Biota in Jervis Bay show
seasonal growth and reproductive patterns, such as increased algal growth and spawning
activities in molluscs in summer (Underwood, 1974). It is therefore likely that the selenium concentrations in biota from Jervis Bay measured in this study are influenced by
factors such as food availability changing temporally with temperature, and growth
rates, reproduction cycles and associated metabolic activities responding to temperature changes and food availability. Laboratory experiments on selenium conducted by
Fowler and Benayoun (1976) showed that increasing the temperature of water from 13 “C to
22°C doubled the selenium concentration factor in Mytilus galloprovincialis. The rise
in temperature probably increased the metabolic rates of these bivalves. Alternatively, a
temperature rise may increase the elimination rate or signal spawning, either of which may
decrease selenium concentration and total selenium body burden in the animals.
Temporal differences in metal concentrations may be a function of mass changes corresponding with reproductive cycles. Growth rates tend to decrease when molluscs reach
sexual maturity because energy is redirected into gamete production at the expense of
energy available for growth (Cossa et al., 1979). Simpson (1979) reports that trace element
variations in Mytifus edulis have been shown to reciprocate seasonal mass variations. This
was the general trend only for 0. angasi (Fig. 5e).
N. atramentosa, B. nanum and M. marginalba spawn through summer, with a peak in
January and finishing by February/March (Underwood, 1974). Hence a mass loss would
be expected over this time unless confounded by mass gain from tissue growth in a possible concomitant growth season (Zwarts, 1991). Although mass losses did not occur,
selenium concentrations and selenium body burdens decreased, suggesting selenium was
lost with mature oocytes.
CONCLUSIONS
The dry mass selenium concentrations determined in molluscs in this study are lower than
those reported in overseas studies of molluscs but do not differ greatly from selenium
concentrations in molluscs reported in other published Australian studies. N. atramentosa
S. Baldwin. W. Maher
260
always had the lowest selenium concentration,
followed usually by A. constricta or
B. nanum, then 0. angasi with M. marginalbu having the highest selenium concentrations.
The distribution
of selenium concentrations
generally exhibited positive skewness and
selenium concentrations
did not have any consistent relationship
with mass or length of
the species.
Significant variation in selenium concentration
existed on all spatial scales (Location,
Site) for all species with the exception of 0. ungasi. All the species showed significant
temporal variation in selenium concentration
and selenium body burdens but there were
no consistent site trends through time or relationships
with mass. Lowest selenium concentrations
were associated with the high body tissue mass in 0. angusi, and spawning in
N. atramentosa, B. nanurn and M. marginalbu.
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