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Metals and organochlorines in small cetaceans stranded on the east coast of Australia
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Baseline / Marine Pollution Bulletin 46 (2003) 1200–1211
Metals and organochlorines in small cetaceans stranded on the east coast of Australia R.J. Law a
a,*
, R.J. Morris b, C.R. Allchin a, B.R. Jones a, M.D. Nicholson
c
CEFAS Burnham Laboratory, Centre for Environment, Fisheries and Aquaculture Science, Remembrance Avenue, Burnham-on-Crouch, Essex CM0 8HA, UK b Department of Anatomy, University of Queensland, Brisbane 4067, Australia c CEFAS Lowestoft Laboratory, Pakefield Road, Lowestoft, Suffolk NR33 0HT, UK
As top predators, marine mammals can accumulate high concentrations of certain contaminants from their diet. It has been suggested that some of these contaminants may act to compromise the immune function of seals and dolphins, thereby rendering them more likely to infection, and this may have been a factor in a number of epizootics which have affected these animals in recent years (de Swart et al., 1996). Recent studies in the UK have also shown statistically significant associations between tissue concentrations of both mercury and chlorobiphenyls in harbour porpoises (Phocoena phocoena) and death from infectious disease (Bennett et al., 2001; Jepson et al., 1999). Contaminant concentrations in cetaceans are related both to the composition of their diet, and to its source relative to inputs from both natural and anthropogenic inputs. It is useful, therefore, to benchmark levels found in cetaceans from the UK against those found elsewhere. Some data are available from Arctic waters and the Pacific Ocean, but few recent data have been published for small cetaceans from Australian waters (Kemper et al., 1994; Vetter et al., 2001). Although lower contaminant levels are generally found in remote sites, there seem to be no entirely pristine areas remaining as transport mechanisms operate globally via the atmosphere, especially for organochlorine compounds (Bignert et al., 1998). In this study we present the analyses of tissue samples taken opportunistically from three species of small cetaceans either stranded, or caught in shark nets, on the east coast of Australia. The three species involved have different behaviours and different patterns of feeding, illustrating varying patterns of uptake of anthropogenic pollutants in these waters. Groups of the inshore form of the bottlenose dolphin (Tursiops truncatus aduncus) found off the east coast of Australia tend to be resident in a particular coastal area. They live and feed close inshore, often spending considerable time in the numerous coastal bays which are partly enclosed by sand islands and sand spits. Their diet comprises a wide range of inshore species; benthic and midwater fish, benthic
* Corresponding author. Tel.: +44-1621-787271; fax: +44-1621785852/784989. E-mail address: [email protected] (R.J. Law).
invertebrates, squid and octopi. In contrast, common dolphins (Delphinus delphis) are mainly pelagic but are often seen close inshore in these waters, sometimes coming right into the coastal bays. Whilst they may be regular visitors to the inshore areas, they could not be considered as even semi-residents. Their diet would be mainly near surface pelagic, probably dominated by schooling fish and squid. Much less is known of the melon-headed whales (Peponocephala electra). They are rarely seen in the inshore waters of the East Australian coast, being almost entirely pelagic and feeding on oceanic squid and fish species from a variety of depths (Evans, 1987; Martin, 1990). The samples obtained for this study were as follows: RJM-02 was a lactating adult female bottlenose dolphin (inshore form) which had been caught in shark nets off the Gold Coast, SE Queensland, and drowned. The animal appeared healthy, with blubber thickness 11–18 mm along the ventral midline. All superficial injuries were consistent with entanglement in a net and there was no other obvious gross pathology. RJM-03 was a young calf bottlenose dolphin (inshore form) which live stranded on the inshore side of the sand spits which separate Gippsland Lakes, Victoria, from the ocean. The calf was taken to Sea World on the Gold Coast but died soon after its arrival. RJM-04 was an immature, female common dolphin found washed up on Mermaid Beach, Gold Coast in SE Queensland. The animal appeared healthy, with blubber thickness of 11–15 mm along the ventral midline. Skin markings appeared to result from ‘‘rope burns’’ and, without any other obvious pathology on what appeared to be a robust carcass, the conclusion was that the animal had become entangled in the shark nets off the beach and died. RJM-05 was an adult, female melon-headed whale which live stranded on the ocean side of Fraser Island in SE Queensland. The animal was taken to Sea World, but died soon after its arrival. This female was believed to have been a member of a group of melon-headed whales which mass stranded three weeks later at Point Plomer. RJM-06 and RJM-07 were adult melon-headed whales, male and female respectively, which were part of a mass stranding on the beach near Point Plomer in northern New South Wales. The biological information on the samples, together with their locations, is summarised in
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Table 1 List of marine mammals from which samples were analysed with biological information Species
Ref. no.
Sex
Age
Length (cm)
Date found
Location
Position
Bottlenose dolphin Bottlenose dolphin Common dolphin Melon-headed whale Melon-headed whale Melon-headed whale
RJM-02 RJM-03 RJM-04 RJM-05 RJM-06 RJM-07
F F F F M F
Adult Calf Juvenile Adult Adult Adult
212 130 118 225 241 235
10/10/95 19/01/96 18/09/95 16/12/95 09/01/96 09/01/96
Gold Coast, Mermaid Beach Gippsland Lake Gold Coast, Main Beach Fraser Island Point Plomer, NSW Point Plomer, NSW
27°590 37°560 28°030 25°150 31°200 31°200
S S S S S S
153°260 147°510 153°260 153°100 152°580 152°580
E E E E E E
analyses were conducted under an analytical quality protocol requiring the analysis of blanks and reference materials alongside each batch of samples. Further details of method performance are given elsewhere (Law et al., 1991; Law, 1994; Law et al., 1997). The results of the analyses are presented in Tables 2–4. The concentrations of trace elements in liver and kidney samples are given in Table 2. Except for Cd, concentrations were, as usual, higher in all cases in liver than in kidney. Transplacental transfer of Cd to calves is low, and the lowest Cd concentrations were seen in a bottlenose dolphin calf and a juvenile common dolphin. The highest concentrations (46–69 mg kg1 wet weight in kidney) were seen in adult melon-headed whales, reflecting the dominance of squid in their diet (Caurant and Amiard-Triquet, 1995; Law, 1996). Hg concentrations were also low in the young animals (0.72 and 0.85 mg kg1 wet weight in liver), with higher concentrations in adults, up to 141 mg kg1 wet weight in the liver of one of the melon-headed whales. Molar ratios of Hg:Se in liver ranged from 0.19 to 1.05, reflecting the conversion by these animals of methylmercury to an inert mineral so as to reduce its toxicity (Law, 1996; Law et al., 1997). The concentration ranges of Cr, Ni, Cu, Zn, and As, were within those reported previously for small cetaceans from the UK and other areas (Law, 1996), and concentrations of Pb were low or undetectable.
Table 1. All of the animals were stranded between September 1995 and January 1996. Tissue samples were analysed for a range of trace elements, organochlorine pesticides and chlorobiphenyl congeners according to previously established and fully validated protocols. The trace elements determined in liver and kidney samples were Cr, Ni, Cu, Zn, As, Se, Ag, Cd, Hg and Pb. Determinations were made using established methodology based upon nitric acid digestion with microwave heating followed (except for mercury) by analysis using inductively coupled plasma/mass spectrometry. Mercury was analysed using atomic fluorescence detection, following reduction with tin(II) chloride (Jones and Laslett, 1994). Blubber and melon samples, and one milk sample, were analysed for organochlorine pesticides and metabolites, and a range of 25 chlorobiphenyl (CB) congeners, using established methodology based upon analysis by gas chromatography with electron-capture detection (Allchin et al., 1989). This method was modified in the light of the recommendations which followed the intercomparison programme organised under the auspices of the International Council for the Exploration of the Sea (de Boer et al., 1992, 1994; de Boer and van der Meer, 1998), and has been further validated for the analysis of biological tissues by participation in the QUASIMEME laboratory proficiency scheme (de Boer and Wells, 1997). All
Table 2 Concentrations of trace elements in liver and kidney tissue (mg kg1 wet weight) Ref. no.
Tissue
TS%a
Cr
Ni
Cu
Zn
As
Se
Ag
Cd
Hg
Pb
Hg:Seb
RJM-02 RJM-03 RJM-04 RJM-05 RJM-06 RJM-07
Liver Liver Liver Liver Liver Liver
32.9 36.9 25.2 31.0 26.4 24.5
1.2 0.97 0.1 0.36 0.15 0.41
0.56 0.12 <0.04 <0.05 <0.05 0.05
8.5 18 11 2.1 4.4 4.9
41 144 77 22 40 47
0.76 0.2 0.32 0.3 0.32 0.75
12 1.5 1.6 6.2 7.9 58
0.54 <0.01 0.05 0.46 0.6 1.6
3.7 0.07 0.02 12 8.0 21
32 0.72 0.85 13 14 141
0.17 0.04 <0.04 <0.04 0.1 <0.04
1.05 0.19 0.21 0.83 0.70 0.96
RJM-02 RJM-03 RJM-04 RJM-05 RJM-06 RJM-07
Kidney Kidney Kidney Kidney Kidney Kidney
24.5 19.6 23.3 19.7 20.1 20.7
0.18 0.11 0.62 0.14 0.25 0.88
<0.04 <0.04 0.25 <0.04 <0.04 0.48
4.7 10 3.9 2.9 2.4 2.4
26 40 20 27 27 30
0.5 0.14 0.36 0.21 0.29 0.2
3.4 1.9 2.6 3.4 4.0 3.5
0.14 0.03 <0.01 0.15 0.03 0.02
15 <0.002 0.07 69 46 61
2.0 0.27 0.11 3.8 2.6 5.1
<0.03 0.04 0.05 <0.03 <0.03 <0.04
0.23 0.06 0.02 0.44 0.26 0.57
a b
TS%: total solids content (%). Molar ratio of mercury and selenium concentrations.
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Baseline / Marine Pollution Bulletin 46 (2003) 1200–1211
Table 3 Concentrations of organochlorine pesticides in samples of blubber, melon and milk (mg kg1 wet weight) Ref. no.
Tissue
%HEL
a-HCH
c-HCH
HCB
p; p0 -DDE
p; p0 -TDE
p; p0 -DDT
Dieldrin
P
RJM-02 RJM-02 RJM-03 RJM-04 RJM-04 RJM-05 RJM-05 RJM-06 RJM-06 RJM-07 RJM-07 RJM-02 RJM-02 RJM-03 RJM-02
Lateral blubber Dorsal blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Surface melon Deep melon Surface melon Milk
61 49 32 80 77 16 9.6 34 30 40 33 86 72 69 21
<0.001 0.001 <0.001 <0.001 <0.001 <0.001 0.008 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001
<0.001 <0.001 <0.001 <0.001 <0.001 <0.001 0.008 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001
<0.001 0.001 0.033 0.036 0.038 0.057 0.031 0.075 0.056 0.038 0.029 0.003 0.003 0.058 <0.001
0.72 0.69 0.2 0.43 0.36 0.61 0.58 0.52 0.47 0.21 0.2 2.2 1.6 0.19 0.07
0.049 0.033 0.02 0.041 0.058 0.094 0.062 0.092 0.086 0.035 0.032 <0.001 <0.001 <0.001 0.004
0.01 0.044 0.049 0.068 0.13 0.29 0.18 0.25 0.24 0.1 0.081 0.053 <0.001 <0.001 <0.001
0.032 0.059 0.045 0.1 0.14 0.074 0.12 0.077 0.078 0.039 0.033 0.015 0.022 0.055 0.009
0.779 0.767 0.269 0.539 0.548 0.994 0.822 0.862 0.796 0.345 0.313 2.253 1.6 0.19 0.074
DDT
DDE/ P DDT 0.92 0.90 0.74 0.80 0.66 0.61 0.71 0.60 0.59 0.61 0.64 0.98 1.00 1.00 0.95
Table 4 Concentrations of chlorobiphenyls in samples of blubber, melon and milk (mg kg1 wet weight) Ref. no.
Tissue
%HEL
CB18
CB31
CB28
CB52
CB49
CB47
CB44
CB66
RJM-02 RJM-02 RJM-03 RJM-04 RJM-04 RJM-05 RJM-05 RJM-06 RJM-06 RJM-07 RJM-07 RJM-02 RJM-02 RJM-03 RJM-02
Lateral blubber Dorsal blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Surface melon Deep melon Surface melon Milk
61 49 32 80 77 16 9.6 34 30 40 33 86 72 69 21
<0.001 <0.001 0.001 <0.001 <0.001 0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001
<0.001 <0.001 0.027 <0.001 0.003 0.007 <0.001 0.009 0.007 0.006 0.005 <0.001 <0.001 0.02 <0.001
<0.001 <0.001 <0.001 <0.001 0.001 <0.001 0.002 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 0.004 <0.001
<0.001 0.006 0.002 <0.001 0.006 0.004 0.002 0.004 0.003 0.002 0.002 <0.001 <0.001 0.004 <0.001
0.015 <0.001 <0.001 0.029 <0.001 0.004 <0.001 <0.001 <0.001 <0.001 <0.001 0.027 0.018 <0.001 <0.001
<0.001 0.004 <0.001 0.002 0.007 0.002 0.049 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001
<0.001 0.001 0.05 0.014 0.017 0.014 0.006 0.017 0.015 0.009 0.007 <0.001 <0.001 0.053 <0.001
CB149
CB118
CB153
CB105
CB141
0.082 0.047 <0.001 0.17 <0.001 0.031 0.023 <0.001 0.023 <0.001 <0.001 0.27 0.18 <0.001 0.004
0.09 0.068 0.26 0.19 0.2 0.086 0.069 0.088 0.086 0.042 0.038 0.28 0.19 0.21 0.008
0.37 0.26 0.035 0.13 0.18 0.078 0.06 0.066 0.062 0.026 0.026 0.95 0.7 0.022 0.021
<0.001 0.013 0.004 0.019 0.025 0.008 0.008 0.007 0.007 <0.001 <0.001 0.042 0.026 <0.001 0.002
<0.001 0.001 <0.001 0.004 0.008 0.005 0.003 0.007 0.006 0.005 0.004 <0.001 <0.001 <0.001 <0.001
CB170
CB194
P
P 25CBs
0.088 0.06 0.008 0.024 0.024
0.028 0.022 0.002 <0.001 0.004
0.92 0.69 0.36 0.52 0.65
RJM-02 RJM-02 RJM-03 RJM-04 RJM-04 RJM-05 RJM-05 RJM-06 RJM-06 RJM-07 RJM-07 RJM-02 RJM-02 RJM-03 RJM-02
RJM-02 RJM-02 RJM-03 RJM-04 RJM-04
Lateral blubber Dorsal blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Surface melon Deep melon Surface melon Milk
Lateral blubber Dorsal blubber Dorsal blubber Lateral blubber Dorsal blubber
ICES7
1.38 1.02 0.5 0.89 0.87
CB101
CB110
CB151
<0.001 <0.001 0.008 <0.001 <0.001 0.012 <0.001 0.013 0.012 0.007 0.005 <0.001 <0.001 0.013 <0.001
0.009 0.02 0.011 0.043 0.056 0.024 0.013 0.022 0.019 0.009 0.007 0.055 0.035 0.011 0.003
0.007 <0.001 0.007 0.024 0.031 0.003 0.002 <0.001 0.005 <0.001 0.005 0.026 0.017 <0.001 0.001
<0.001 0.013 0.003 <0.001 0.012 0.009 0.006 0.008 0.007 0.003 0.002 0.033 0.017 0.003 0.001
CB138 CB158
CB187 CB183
CB128
CB156
CB180
0.26 0.2 0.028 0.13 0.15 0.067 0.053 0.058 0.055 0.025 0.023 0.71 0.5 0.025 0.016
0.095 0.074 0.015 0.01 0.035 0.027 0.023 0.024 0.023 0.013 0.012 0.2 0.15 0.009 0.004
0.065 0.029 0.005 0.055 0.026 0.009 0.009 0.011 0.01 0.006 0.005 0.16 0.12 <0.001 0.003
0.025 0.013 0.004 0.011 0.012 0.006 0.005 0.007 0.006 <0.001 0.004 0.056 0.043 <0.001 <0.001
0.19 0.14 0.021 0.029 0.053 0.043 0.041 0.037 0.036 0.019 0.021 0.41 0.28 0.015 0.006
0.022 0.017 0.002 0.009 0.01 0.004 0.002 0.003 0.003 <0.001 0.001 0.065 0.046 <0.001 0.001
0.037 0.031 0.004 <0.001 0.013 0.01 0.009 0.007 0.007 0.003 0.004 0.086 0.06 <0.001 0.001
Baseline / Marine Pollution Bulletin 46 (2003) 1200–1211 Table 4 (continued) Ref. no.
Tissue
CB170
CB194
P
RJM-05 RJM-05 RJM-06 RJM-06 RJM-07 RJM-07 RJM-02 RJM-02 RJM-03 RJM-02
Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Surface melon Deep melon Surface melon Milk
0.014 0.015 0.015 0.014 0.009 0.008 0.19 0.13 0.01 0.003
0.003 0.004 0.002 0.003 0.002 0.003 0.042 0.03 <0.001 <0.001
0.3 0.24 0.28 0.26 0.12 0.12 2.41 1.71 0.29 0.054
ICES7
P
1209
25CBs
0.47 0.4 0.41 0.41 0.19 0.18 3.6 2.54 0.4 0.074
The concentrations of a range of organochlorine pesticides and their metabolites are given in Table 3. Concentrations of a- and P c-HCH, HCB and dieldrin were low in all samples. DDT concentrations ranged from 0.27 to 0.99 mg kg1 wet weight in blubber, 0.19 to 2.3 mg kg1 in melon, and a single value of 0.07 mg kg1 was observed in milk. The predominant compound P present was p; p0 -DDE, and the ratios of DDE/ DDT ranged from 0.6 to 1.0, indicating that this represents historic contamination rather than recent inputs (Aguilar, 1984). The concentrations of the 25 CB congeners determined are given in Table 4. The range of concentrations of the summed congeners (ICES7 CBs and all 25 CBs determined) was 0.12–0.92 and 0.18–1.38 mg kg1 wet weight respectively in blubber, and 0.29–2.41 and 0.4– 3.6 mg kg1 wet weight respectively in melon. CB concentrations were higher in the surface of the melon of a bottlenose dolphin (RJM-02) than in the deeper tissue, but the deep melon sample taken from a calf (RJM-03) proved to consist entirely of connective tissue with a negligible lipid content and so no CB determination P could be made. 25CB concentrations (sum of all 25 congeners) in samples of dorsal and lateral blubber generally agreed well, with a mean difference between pairs of samples of 12% and a range of 0–30% when expressed on a lipid basis. The greatest difference was seen in RJM-05, an adult melon-headed whale with a blubber lipid content of only 10–16% indicating a starved animal. In the other animals, blubber lipid contents varied from 30% to 80%, and the concentration differences between replicates ranged from 0% to 15%. It has been suggested that the concentration ranges for homeostatic control of Cu and Zn in marine mammal livers may lie within, or close to, ranges of 3–30 mg kg1 and 20–100 mg kg1 wet weight respectively. In these samples the respective ranges are 2.1–18 mg kg1 and 22–144 mg kg1 wet weight, the highest value for Zn occurring in a bottlenose dolphin calf (RJM-03). Cd concentrations in kidney are below the critical concentration of 200 mg kg1 wet weight, a level associated with renal damage in humans and other mammals (WHO, 1992), the highest value reported in this study
being 69 mg kg1 wet weight. Elevated Cd concentrations deriving from natural sources via dietary uptake have been reported for some remote areas including Northwest Greenland, where kidney concentrations up to 580 mg kg1 have been observed in ringed seal (Phoca hispida) (Dietz et al., 1998). In the Faroe Islands, concentrations up to 78 mg kg1 (similar to the highest value observed in our study) have been reported in longfinned pilot whales (Globicephala melas) (Caurant and Amiard-Triquet, 1995). These authors concluded that pilot whales have a remarkable tolerance to heavy metals, presumably developed in response to the high levels ingested with their major prey, squid. Metals enter the marine environment both naturally as well as from anthropogenic discharges, and so the exposure of marine mammals to metals has occurred throughout history. It is not surprising, therefore, that they have developed mechanisms to mitigate the toxic effects of metals ingested from their prey, such as Cd and Hg (Law, 1996). The highest concentrations of p; p0 -DDE were observed in the melon samples from the inshore adult bottlenose dolphin (RJM-02), 1.6 and 2.2 mg kg1 wet weight. The melon is a unique physiological organ. It represents a major lipid reservoir, but unlike the blubber is not remobilised in order to provide energy. The melon has evolved specifically for use in the dolphins acoustic sensory faculty, whereas the blubber has both a thermoregulatory function, and provides a fat store which can be utilised during periods of food shortage. The lipid initially deposited in the melon is synthesised de novo at an early stage in the animals life, and then enlarged during growth and maintained throughout its life. It may therefore represent a ‘‘memory’’ of the uptake of lipophilic contaminants over time, particularly if the structure is maintained during growth and the lipid deposited layerwise. In the case of this animal, p; p0 DDE represents 98–100% of the total DDT burden in the melon as against 90–92% in its blubber; in the melon of the calf (RJM-03) the corresponding values are 100% and 74%, suggesting a greater degree of metabolism and a longer residence time in the melon than the blubber in both cases.
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Baseline / Marine Pollution Bulletin 46 (2003) 1200–1211
Table 5 Comparison of data for selected organochlorine compounds in bottlenose dolphin blubber from this study and Vetter et al. (2001) (lg kg1 on a lipid basis) Compound
Adult female
Calf
Adult female #1
Adult female #2
Adult male #3
Adult male #4
CB138 CB153 CB180 p; p0 -DDE p; p0 -TDE p; p0 -DDT
408 531 286 1410 67 90
88 109 66 625 63 153
140 229 100 420 173 89
352 540 276 1680 86 126
6390 8810 4190 52,400 618 515
1240 2150 1370 11,300 223 240
Blubber CB concentrations were low relative to those seen P in many small cetaceans from the UK, with 25CB concentrations ranging from 0.18 to 1.38 mg kg1 wet weight. The corresponding ranges for 35 common dolphins, 2 bottlenose dolphins, and 98 porpoises (P. phocoena) from the UK were 2.3–84, 11 and 119, and 0.12–90 mg kg1 wet weight respectively (Law, 1994). It seems therefore that small cetaceans from the Queensland coast are relatively lightly contaminated with CBs when compared with animals from the UK. Principal component analysis of the CB data demonstrated that the major influence on the first component, accounting for 95% of the variability in the data, stemmed from CB138, CB153 and CB180, which are recalcitrant congeners and those normally accumulated to highest concentration. This primarily reflects quantitative differences in concentrations between CBs in the adult bottlenose dolphin and the other animals. The second component was driven primarily by the concentrations of CB118. This difference was investigated further by normalising the CB concentrations in each case to CB153 (generally the most abundant congener) and repeating the statistical analysis. In this case the first component explained some 97% of the variation in relative CB concentrations, and the bottlenose dolphin calf was highlighted as distinct from the other animals as a result of the higher concentrations of some lower chlorinated CBs (CB31, CB44, CB118) observed in the calf. These differences between the relative CB concentrations in the bottlenose dolphin calf (RJM-03) and the other animals may reflect differences in metabolic capacity, as CB118 is a type III congener with vicinal hydrogen atoms in the ortho- and meta-positions in combination with 1 ortho-chlorine atom, and so can be metabolised by many species of marine mammals (Boon et al., 1997). Table 5 shows a comparison of data for selected organochlorine pesticides and CBs, expressed on a lipid basis, for bottlenose dolphins both from this study and from that of Vetter et al. (2001). The lowest concentrations are observed in the calf, and the highest in the two adult males. Adult females show intermediate concentrations as a result of their ability to reduce their body burden by transfer of lipophilic contaminants to their offspring both across the placenta and in milk.
Acknowledgement This work was funded by the Department for Environment, Food and Rural Affairs as part of its programme of marine environmental research.
References P Aguilar, A., 1984. Relationship of DDE/ DDT in marine mammals to the chronology of DDT input into the ecosystem. Can. J. Fish. Aquat. Sci. 41, 840–844. Allchin, C.R., Kelly, C.A., Portmann, J.E., 1989. Methods of analysis for chlorinated hydrocarbons in marine and other samples. Aquatic Environment Protection: Analytical Method. Ministry of Agriculture, Fisheries and Food, Directorate of Fisheries Research, Lowestoft, (6), 25 pp. Bennett, P.M., Jepson, P.D., Law, R.J., Jones, B.R., Kuiken, T., Baker, J.R., Rogan, E., Kirkwood, J.K., 2001. Exposure to heavy metals and infectious disease mortality in harbour porpoises from England and Wales. Environ. Pollut. 112, 33–40. Bignert, A., Olsson, M., Persson, W., Jensen, S., Zakrisson, S., Litzen, K., Eriksson, U., H€aggberg, L., Alsberg, T., 1998. Temporal trends of organochlorines in Northern Europe, 1967–1995. Relation to global fractionation, leakage from sediments, and international measures. Environ. Pollut. 99, 177–198. Boon, J.P., van der Meer, J., Allchin, C.R., Law, R.J., Klungsyr, J., Leonards, P.E.G., Spliid, H., Storr-Hansen, E., Wells, D.E., McKenzie, C., 1997. Concentration dependent changes of PCB patterns in fish-eating mammals. Structural evidence for induction of cytochrome P450. Arch. Environ. Contam. Toxicol. 33, 298–311. Caurant, F., Amiard-Triquet, C., 1995. Cadmium contamination in pilot whales Globicephala melas: source and potential hazard to the species. Mar. Pollut. Bull. 30, 207–210. de Boer, J., van der Meer, J., 1998. Report on the results of the ICES/ IOC/OSPARCOM intercomparison exercise on the determination of chlorobiphenyl congeners in marine media––steps 3a, 3b, 4 and assessment. ICES Cooperative Research Report, 226. International Council for the Exploration of the Sea, Copenhagen, Denmark. de Boer, J., Wells, D.E., 1997. Chlorobiphenyls and organochlorine pesticides in fish and sediments––Three years of QUASIMEME laboratory performance studies. Mar. Pollut. Bull. 35, 52–63. de Boer, J., Duinker, J.C., Calder, J.A., van der Meer, J., 1992. Interlaboratory study on the analysis of chlorobiphenyl congeners. JAOAC 75, 1054–1062. de Boer, J., van der Meer, J., Reuterg ardh, L., Calder, J.A., 1994. Interlaboratory study on the analysis of chlorobiphenyls in cleaned-up seal blubber and marine sediment extracts. JAOAC 77, 1411–1422. de Swart, R.L., Ross, P.S., Vos, J.G., Osterhaus, A.D.M.E., 1996. Impaired immunity in harbour seals (Phoca vitulina) exposed to
Baseline / Marine Pollution Bulletin 46 (2003) 1200–1211 bioaccumulated environmental contaminants: review of a long-term feeding study. Environ. Health Perspect. 104 (Suppl. 4), 823–828. Dietz, R., Nrgaard, J., Hansen, J.C., 1998. Have Arctic marine mammals adapted to high cadmium levels? Mar. Pollut. Bull. 36, 490–492. Evans, P.G.H., 1987. The Natural History of Whales and Dolphins. Christopher Helm Ltd., Bromley, UK. ISBN 0-7470-0800-0. Jepson, P.D., Bennett, P.M., Allchin, C.R., Law, R.J., Kuiken, T., Baker, J.R., Rogan, E., Kirkwood, J.K., 1999. Investigating potential associations between chronic exposure to polychlorinated biphenyls and infectious disease mortality in harbour porpoises from England and Wales. Sci. Total Environ. 243/244, 339–348. Jones, B.R., Laslett, R.E., 1994. Methods for the analysis of trace metals in marine and other samples. Aquatic Environment Protection: Analytical Method. Ministry of Agriculture, Fisheries and Food, Directorate of Fisheries Research, Lowestoft, (11), 29 pp. Kemper, C., Gibbs, P., Obendorf, D., Marvanek, S., Lenghaus, C., 1994. A review of heavy metal and organochlorine levels in marine mammals in Australia. Sci. Total Environ. 154, 129–139. Law, R.J., 1994. (Compiler). Collaborative UK marine mammal project: summary of data produced 1988–1992. Fisheries Research Technical Report, Ministry of Agriculture, Fisheries and Food, Directorate of Fisheries Research, Lowestoft, (97), 42 pp.
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Law, R.J., 1996. Metals in marine mammals. In: Beyer, W.N., Heinz, G.H., Redmon-Norwood, A.W. (Eds.), Environmental Contaminants in Wildlife: Interpreting Tissue Concentrations. CRC Press, Inc, Boca Raton, USA, pp. 357–376, ISBN 1-56670071-X. Law, R.J., Fileman, C.F., Hopkins, A.D., Baker, J.R., Harwood, J., Jackson, D.B., Kennedy, S., Martin, A.R., Morris, R.J., 1991. Concentrations of trace metals in the livers of marine mammals (seals, porpoises and dolphins) from waters around the British Isles. Mar. Pollut. Bull. 22, 183–191. Law, R.J., Allchin, C.R., Jones, B.R., Jepson, P.D., Baker, J.R., Spurrier, C.J.H., 1997. Metals and organochlorines in tissues of a Blainvilles beaked whale (Mesoplodon densirostris) and a killer whale (Orcinus orca) stranded in the UK. Mar. Pollut. Bull. 34, 208–212. Martin, A.R., 1990. Whales and Dolphins. Salamander Books Ltd., London, ISBN 0-86101-488-X. Vetter, W., Scholz, E., Gaus, C., Muller, J.F., Haynes, D., 2001. Anthropogenic and natural organohalogen compounds in blubber of dolphins and dugongs (Dugong dugon) from northeastern Australia. Arch. Environ. Contam. Toxicol. 41, 221–231. WHO, 1992. Cadmium. Environmental Health Criteria, vol. 134. World Health Organisation, Geneva.
0025-326X/$ - see front matter Crown Copyright Ó 2003 Published by Elsevier Ltd. All rights reserved. doi:10.1016/S0025-326X(03)00220-0
Baseline / Marine Pollution Bulletin 46 (2003) 1200–1211
Metals and organochlorines in small cetaceans stranded on the east coast of Australia R.J. Law a
a,*
, R.J. Morris b, C.R. Allchin a, B.R. Jones a, M.D. Nicholson
c
CEFAS Burnham Laboratory, Centre for Environment, Fisheries and Aquaculture Science, Remembrance Avenue, Burnham-on-Crouch, Essex CM0 8HA, UK b Department of Anatomy, University of Queensland, Brisbane 4067, Australia c CEFAS Lowestoft Laboratory, Pakefield Road, Lowestoft, Suffolk NR33 0HT, UK
As top predators, marine mammals can accumulate high concentrations of certain contaminants from their diet. It has been suggested that some of these contaminants may act to compromise the immune function of seals and dolphins, thereby rendering them more likely to infection, and this may have been a factor in a number of epizootics which have affected these animals in recent years (de Swart et al., 1996). Recent studies in the UK have also shown statistically significant associations between tissue concentrations of both mercury and chlorobiphenyls in harbour porpoises (Phocoena phocoena) and death from infectious disease (Bennett et al., 2001; Jepson et al., 1999). Contaminant concentrations in cetaceans are related both to the composition of their diet, and to its source relative to inputs from both natural and anthropogenic inputs. It is useful, therefore, to benchmark levels found in cetaceans from the UK against those found elsewhere. Some data are available from Arctic waters and the Pacific Ocean, but few recent data have been published for small cetaceans from Australian waters (Kemper et al., 1994; Vetter et al., 2001). Although lower contaminant levels are generally found in remote sites, there seem to be no entirely pristine areas remaining as transport mechanisms operate globally via the atmosphere, especially for organochlorine compounds (Bignert et al., 1998). In this study we present the analyses of tissue samples taken opportunistically from three species of small cetaceans either stranded, or caught in shark nets, on the east coast of Australia. The three species involved have different behaviours and different patterns of feeding, illustrating varying patterns of uptake of anthropogenic pollutants in these waters. Groups of the inshore form of the bottlenose dolphin (Tursiops truncatus aduncus) found off the east coast of Australia tend to be resident in a particular coastal area. They live and feed close inshore, often spending considerable time in the numerous coastal bays which are partly enclosed by sand islands and sand spits. Their diet comprises a wide range of inshore species; benthic and midwater fish, benthic
* Corresponding author. Tel.: +44-1621-787271; fax: +44-1621785852/784989. E-mail address: [email protected] (R.J. Law).
invertebrates, squid and octopi. In contrast, common dolphins (Delphinus delphis) are mainly pelagic but are often seen close inshore in these waters, sometimes coming right into the coastal bays. Whilst they may be regular visitors to the inshore areas, they could not be considered as even semi-residents. Their diet would be mainly near surface pelagic, probably dominated by schooling fish and squid. Much less is known of the melon-headed whales (Peponocephala electra). They are rarely seen in the inshore waters of the East Australian coast, being almost entirely pelagic and feeding on oceanic squid and fish species from a variety of depths (Evans, 1987; Martin, 1990). The samples obtained for this study were as follows: RJM-02 was a lactating adult female bottlenose dolphin (inshore form) which had been caught in shark nets off the Gold Coast, SE Queensland, and drowned. The animal appeared healthy, with blubber thickness 11–18 mm along the ventral midline. All superficial injuries were consistent with entanglement in a net and there was no other obvious gross pathology. RJM-03 was a young calf bottlenose dolphin (inshore form) which live stranded on the inshore side of the sand spits which separate Gippsland Lakes, Victoria, from the ocean. The calf was taken to Sea World on the Gold Coast but died soon after its arrival. RJM-04 was an immature, female common dolphin found washed up on Mermaid Beach, Gold Coast in SE Queensland. The animal appeared healthy, with blubber thickness of 11–15 mm along the ventral midline. Skin markings appeared to result from ‘‘rope burns’’ and, without any other obvious pathology on what appeared to be a robust carcass, the conclusion was that the animal had become entangled in the shark nets off the beach and died. RJM-05 was an adult, female melon-headed whale which live stranded on the ocean side of Fraser Island in SE Queensland. The animal was taken to Sea World, but died soon after its arrival. This female was believed to have been a member of a group of melon-headed whales which mass stranded three weeks later at Point Plomer. RJM-06 and RJM-07 were adult melon-headed whales, male and female respectively, which were part of a mass stranding on the beach near Point Plomer in northern New South Wales. The biological information on the samples, together with their locations, is summarised in
Baseline / Marine Pollution Bulletin 46 (2003) 1200–1211
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Table 1 List of marine mammals from which samples were analysed with biological information Species
Ref. no.
Sex
Age
Length (cm)
Date found
Location
Position
Bottlenose dolphin Bottlenose dolphin Common dolphin Melon-headed whale Melon-headed whale Melon-headed whale
RJM-02 RJM-03 RJM-04 RJM-05 RJM-06 RJM-07
F F F F M F
Adult Calf Juvenile Adult Adult Adult
212 130 118 225 241 235
10/10/95 19/01/96 18/09/95 16/12/95 09/01/96 09/01/96
Gold Coast, Mermaid Beach Gippsland Lake Gold Coast, Main Beach Fraser Island Point Plomer, NSW Point Plomer, NSW
27°590 37°560 28°030 25°150 31°200 31°200
S S S S S S
153°260 147°510 153°260 153°100 152°580 152°580
E E E E E E
analyses were conducted under an analytical quality protocol requiring the analysis of blanks and reference materials alongside each batch of samples. Further details of method performance are given elsewhere (Law et al., 1991; Law, 1994; Law et al., 1997). The results of the analyses are presented in Tables 2–4. The concentrations of trace elements in liver and kidney samples are given in Table 2. Except for Cd, concentrations were, as usual, higher in all cases in liver than in kidney. Transplacental transfer of Cd to calves is low, and the lowest Cd concentrations were seen in a bottlenose dolphin calf and a juvenile common dolphin. The highest concentrations (46–69 mg kg1 wet weight in kidney) were seen in adult melon-headed whales, reflecting the dominance of squid in their diet (Caurant and Amiard-Triquet, 1995; Law, 1996). Hg concentrations were also low in the young animals (0.72 and 0.85 mg kg1 wet weight in liver), with higher concentrations in adults, up to 141 mg kg1 wet weight in the liver of one of the melon-headed whales. Molar ratios of Hg:Se in liver ranged from 0.19 to 1.05, reflecting the conversion by these animals of methylmercury to an inert mineral so as to reduce its toxicity (Law, 1996; Law et al., 1997). The concentration ranges of Cr, Ni, Cu, Zn, and As, were within those reported previously for small cetaceans from the UK and other areas (Law, 1996), and concentrations of Pb were low or undetectable.
Table 1. All of the animals were stranded between September 1995 and January 1996. Tissue samples were analysed for a range of trace elements, organochlorine pesticides and chlorobiphenyl congeners according to previously established and fully validated protocols. The trace elements determined in liver and kidney samples were Cr, Ni, Cu, Zn, As, Se, Ag, Cd, Hg and Pb. Determinations were made using established methodology based upon nitric acid digestion with microwave heating followed (except for mercury) by analysis using inductively coupled plasma/mass spectrometry. Mercury was analysed using atomic fluorescence detection, following reduction with tin(II) chloride (Jones and Laslett, 1994). Blubber and melon samples, and one milk sample, were analysed for organochlorine pesticides and metabolites, and a range of 25 chlorobiphenyl (CB) congeners, using established methodology based upon analysis by gas chromatography with electron-capture detection (Allchin et al., 1989). This method was modified in the light of the recommendations which followed the intercomparison programme organised under the auspices of the International Council for the Exploration of the Sea (de Boer et al., 1992, 1994; de Boer and van der Meer, 1998), and has been further validated for the analysis of biological tissues by participation in the QUASIMEME laboratory proficiency scheme (de Boer and Wells, 1997). All
Table 2 Concentrations of trace elements in liver and kidney tissue (mg kg1 wet weight) Ref. no.
Tissue
TS%a
Cr
Ni
Cu
Zn
As
Se
Ag
Cd
Hg
Pb
Hg:Seb
RJM-02 RJM-03 RJM-04 RJM-05 RJM-06 RJM-07
Liver Liver Liver Liver Liver Liver
32.9 36.9 25.2 31.0 26.4 24.5
1.2 0.97 0.1 0.36 0.15 0.41
0.56 0.12 <0.04 <0.05 <0.05 0.05
8.5 18 11 2.1 4.4 4.9
41 144 77 22 40 47
0.76 0.2 0.32 0.3 0.32 0.75
12 1.5 1.6 6.2 7.9 58
0.54 <0.01 0.05 0.46 0.6 1.6
3.7 0.07 0.02 12 8.0 21
32 0.72 0.85 13 14 141
0.17 0.04 <0.04 <0.04 0.1 <0.04
1.05 0.19 0.21 0.83 0.70 0.96
RJM-02 RJM-03 RJM-04 RJM-05 RJM-06 RJM-07
Kidney Kidney Kidney Kidney Kidney Kidney
24.5 19.6 23.3 19.7 20.1 20.7
0.18 0.11 0.62 0.14 0.25 0.88
<0.04 <0.04 0.25 <0.04 <0.04 0.48
4.7 10 3.9 2.9 2.4 2.4
26 40 20 27 27 30
0.5 0.14 0.36 0.21 0.29 0.2
3.4 1.9 2.6 3.4 4.0 3.5
0.14 0.03 <0.01 0.15 0.03 0.02
15 <0.002 0.07 69 46 61
2.0 0.27 0.11 3.8 2.6 5.1
<0.03 0.04 0.05 <0.03 <0.03 <0.04
0.23 0.06 0.02 0.44 0.26 0.57
a b
TS%: total solids content (%). Molar ratio of mercury and selenium concentrations.
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Table 3 Concentrations of organochlorine pesticides in samples of blubber, melon and milk (mg kg1 wet weight) Ref. no.
Tissue
%HEL
a-HCH
c-HCH
HCB
p; p0 -DDE
p; p0 -TDE
p; p0 -DDT
Dieldrin
P
RJM-02 RJM-02 RJM-03 RJM-04 RJM-04 RJM-05 RJM-05 RJM-06 RJM-06 RJM-07 RJM-07 RJM-02 RJM-02 RJM-03 RJM-02
Lateral blubber Dorsal blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Surface melon Deep melon Surface melon Milk
61 49 32 80 77 16 9.6 34 30 40 33 86 72 69 21
<0.001 0.001 <0.001 <0.001 <0.001 <0.001 0.008 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001
<0.001 <0.001 <0.001 <0.001 <0.001 <0.001 0.008 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001
<0.001 0.001 0.033 0.036 0.038 0.057 0.031 0.075 0.056 0.038 0.029 0.003 0.003 0.058 <0.001
0.72 0.69 0.2 0.43 0.36 0.61 0.58 0.52 0.47 0.21 0.2 2.2 1.6 0.19 0.07
0.049 0.033 0.02 0.041 0.058 0.094 0.062 0.092 0.086 0.035 0.032 <0.001 <0.001 <0.001 0.004
0.01 0.044 0.049 0.068 0.13 0.29 0.18 0.25 0.24 0.1 0.081 0.053 <0.001 <0.001 <0.001
0.032 0.059 0.045 0.1 0.14 0.074 0.12 0.077 0.078 0.039 0.033 0.015 0.022 0.055 0.009
0.779 0.767 0.269 0.539 0.548 0.994 0.822 0.862 0.796 0.345 0.313 2.253 1.6 0.19 0.074
DDT
DDE/ P DDT 0.92 0.90 0.74 0.80 0.66 0.61 0.71 0.60 0.59 0.61 0.64 0.98 1.00 1.00 0.95
Table 4 Concentrations of chlorobiphenyls in samples of blubber, melon and milk (mg kg1 wet weight) Ref. no.
Tissue
%HEL
CB18
CB31
CB28
CB52
CB49
CB47
CB44
CB66
RJM-02 RJM-02 RJM-03 RJM-04 RJM-04 RJM-05 RJM-05 RJM-06 RJM-06 RJM-07 RJM-07 RJM-02 RJM-02 RJM-03 RJM-02
Lateral blubber Dorsal blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Surface melon Deep melon Surface melon Milk
61 49 32 80 77 16 9.6 34 30 40 33 86 72 69 21
<0.001 <0.001 0.001 <0.001 <0.001 0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001
<0.001 <0.001 0.027 <0.001 0.003 0.007 <0.001 0.009 0.007 0.006 0.005 <0.001 <0.001 0.02 <0.001
<0.001 <0.001 <0.001 <0.001 0.001 <0.001 0.002 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 0.004 <0.001
<0.001 0.006 0.002 <0.001 0.006 0.004 0.002 0.004 0.003 0.002 0.002 <0.001 <0.001 0.004 <0.001
0.015 <0.001 <0.001 0.029 <0.001 0.004 <0.001 <0.001 <0.001 <0.001 <0.001 0.027 0.018 <0.001 <0.001
<0.001 0.004 <0.001 0.002 0.007 0.002 0.049 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001
<0.001 0.001 0.05 0.014 0.017 0.014 0.006 0.017 0.015 0.009 0.007 <0.001 <0.001 0.053 <0.001
CB149
CB118
CB153
CB105
CB141
0.082 0.047 <0.001 0.17 <0.001 0.031 0.023 <0.001 0.023 <0.001 <0.001 0.27 0.18 <0.001 0.004
0.09 0.068 0.26 0.19 0.2 0.086 0.069 0.088 0.086 0.042 0.038 0.28 0.19 0.21 0.008
0.37 0.26 0.035 0.13 0.18 0.078 0.06 0.066 0.062 0.026 0.026 0.95 0.7 0.022 0.021
<0.001 0.013 0.004 0.019 0.025 0.008 0.008 0.007 0.007 <0.001 <0.001 0.042 0.026 <0.001 0.002
<0.001 0.001 <0.001 0.004 0.008 0.005 0.003 0.007 0.006 0.005 0.004 <0.001 <0.001 <0.001 <0.001
CB170
CB194
P
P 25CBs
0.088 0.06 0.008 0.024 0.024
0.028 0.022 0.002 <0.001 0.004
0.92 0.69 0.36 0.52 0.65
RJM-02 RJM-02 RJM-03 RJM-04 RJM-04 RJM-05 RJM-05 RJM-06 RJM-06 RJM-07 RJM-07 RJM-02 RJM-02 RJM-03 RJM-02
RJM-02 RJM-02 RJM-03 RJM-04 RJM-04
Lateral blubber Dorsal blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Surface melon Deep melon Surface melon Milk
Lateral blubber Dorsal blubber Dorsal blubber Lateral blubber Dorsal blubber
ICES7
1.38 1.02 0.5 0.89 0.87
CB101
CB110
CB151
<0.001 <0.001 0.008 <0.001 <0.001 0.012 <0.001 0.013 0.012 0.007 0.005 <0.001 <0.001 0.013 <0.001
0.009 0.02 0.011 0.043 0.056 0.024 0.013 0.022 0.019 0.009 0.007 0.055 0.035 0.011 0.003
0.007 <0.001 0.007 0.024 0.031 0.003 0.002 <0.001 0.005 <0.001 0.005 0.026 0.017 <0.001 0.001
<0.001 0.013 0.003 <0.001 0.012 0.009 0.006 0.008 0.007 0.003 0.002 0.033 0.017 0.003 0.001
CB138 CB158
CB187 CB183
CB128
CB156
CB180
0.26 0.2 0.028 0.13 0.15 0.067 0.053 0.058 0.055 0.025 0.023 0.71 0.5 0.025 0.016
0.095 0.074 0.015 0.01 0.035 0.027 0.023 0.024 0.023 0.013 0.012 0.2 0.15 0.009 0.004
0.065 0.029 0.005 0.055 0.026 0.009 0.009 0.011 0.01 0.006 0.005 0.16 0.12 <0.001 0.003
0.025 0.013 0.004 0.011 0.012 0.006 0.005 0.007 0.006 <0.001 0.004 0.056 0.043 <0.001 <0.001
0.19 0.14 0.021 0.029 0.053 0.043 0.041 0.037 0.036 0.019 0.021 0.41 0.28 0.015 0.006
0.022 0.017 0.002 0.009 0.01 0.004 0.002 0.003 0.003 <0.001 0.001 0.065 0.046 <0.001 0.001
0.037 0.031 0.004 <0.001 0.013 0.01 0.009 0.007 0.007 0.003 0.004 0.086 0.06 <0.001 0.001
Baseline / Marine Pollution Bulletin 46 (2003) 1200–1211 Table 4 (continued) Ref. no.
Tissue
CB170
CB194
P
RJM-05 RJM-05 RJM-06 RJM-06 RJM-07 RJM-07 RJM-02 RJM-02 RJM-03 RJM-02
Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Lateral blubber Dorsal blubber Surface melon Deep melon Surface melon Milk
0.014 0.015 0.015 0.014 0.009 0.008 0.19 0.13 0.01 0.003
0.003 0.004 0.002 0.003 0.002 0.003 0.042 0.03 <0.001 <0.001
0.3 0.24 0.28 0.26 0.12 0.12 2.41 1.71 0.29 0.054
ICES7
P
1209
25CBs
0.47 0.4 0.41 0.41 0.19 0.18 3.6 2.54 0.4 0.074
The concentrations of a range of organochlorine pesticides and their metabolites are given in Table 3. Concentrations of a- and P c-HCH, HCB and dieldrin were low in all samples. DDT concentrations ranged from 0.27 to 0.99 mg kg1 wet weight in blubber, 0.19 to 2.3 mg kg1 in melon, and a single value of 0.07 mg kg1 was observed in milk. The predominant compound P present was p; p0 -DDE, and the ratios of DDE/ DDT ranged from 0.6 to 1.0, indicating that this represents historic contamination rather than recent inputs (Aguilar, 1984). The concentrations of the 25 CB congeners determined are given in Table 4. The range of concentrations of the summed congeners (ICES7 CBs and all 25 CBs determined) was 0.12–0.92 and 0.18–1.38 mg kg1 wet weight respectively in blubber, and 0.29–2.41 and 0.4– 3.6 mg kg1 wet weight respectively in melon. CB concentrations were higher in the surface of the melon of a bottlenose dolphin (RJM-02) than in the deeper tissue, but the deep melon sample taken from a calf (RJM-03) proved to consist entirely of connective tissue with a negligible lipid content and so no CB determination P could be made. 25CB concentrations (sum of all 25 congeners) in samples of dorsal and lateral blubber generally agreed well, with a mean difference between pairs of samples of 12% and a range of 0–30% when expressed on a lipid basis. The greatest difference was seen in RJM-05, an adult melon-headed whale with a blubber lipid content of only 10–16% indicating a starved animal. In the other animals, blubber lipid contents varied from 30% to 80%, and the concentration differences between replicates ranged from 0% to 15%. It has been suggested that the concentration ranges for homeostatic control of Cu and Zn in marine mammal livers may lie within, or close to, ranges of 3–30 mg kg1 and 20–100 mg kg1 wet weight respectively. In these samples the respective ranges are 2.1–18 mg kg1 and 22–144 mg kg1 wet weight, the highest value for Zn occurring in a bottlenose dolphin calf (RJM-03). Cd concentrations in kidney are below the critical concentration of 200 mg kg1 wet weight, a level associated with renal damage in humans and other mammals (WHO, 1992), the highest value reported in this study
being 69 mg kg1 wet weight. Elevated Cd concentrations deriving from natural sources via dietary uptake have been reported for some remote areas including Northwest Greenland, where kidney concentrations up to 580 mg kg1 have been observed in ringed seal (Phoca hispida) (Dietz et al., 1998). In the Faroe Islands, concentrations up to 78 mg kg1 (similar to the highest value observed in our study) have been reported in longfinned pilot whales (Globicephala melas) (Caurant and Amiard-Triquet, 1995). These authors concluded that pilot whales have a remarkable tolerance to heavy metals, presumably developed in response to the high levels ingested with their major prey, squid. Metals enter the marine environment both naturally as well as from anthropogenic discharges, and so the exposure of marine mammals to metals has occurred throughout history. It is not surprising, therefore, that they have developed mechanisms to mitigate the toxic effects of metals ingested from their prey, such as Cd and Hg (Law, 1996). The highest concentrations of p; p0 -DDE were observed in the melon samples from the inshore adult bottlenose dolphin (RJM-02), 1.6 and 2.2 mg kg1 wet weight. The melon is a unique physiological organ. It represents a major lipid reservoir, but unlike the blubber is not remobilised in order to provide energy. The melon has evolved specifically for use in the dolphins acoustic sensory faculty, whereas the blubber has both a thermoregulatory function, and provides a fat store which can be utilised during periods of food shortage. The lipid initially deposited in the melon is synthesised de novo at an early stage in the animals life, and then enlarged during growth and maintained throughout its life. It may therefore represent a ‘‘memory’’ of the uptake of lipophilic contaminants over time, particularly if the structure is maintained during growth and the lipid deposited layerwise. In the case of this animal, p; p0 DDE represents 98–100% of the total DDT burden in the melon as against 90–92% in its blubber; in the melon of the calf (RJM-03) the corresponding values are 100% and 74%, suggesting a greater degree of metabolism and a longer residence time in the melon than the blubber in both cases.
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Table 5 Comparison of data for selected organochlorine compounds in bottlenose dolphin blubber from this study and Vetter et al. (2001) (lg kg1 on a lipid basis) Compound
Adult female
Calf
Adult female #1
Adult female #2
Adult male #3
Adult male #4
CB138 CB153 CB180 p; p0 -DDE p; p0 -TDE p; p0 -DDT
408 531 286 1410 67 90
88 109 66 625 63 153
140 229 100 420 173 89
352 540 276 1680 86 126
6390 8810 4190 52,400 618 515
1240 2150 1370 11,300 223 240
Blubber CB concentrations were low relative to those seen P in many small cetaceans from the UK, with 25CB concentrations ranging from 0.18 to 1.38 mg kg1 wet weight. The corresponding ranges for 35 common dolphins, 2 bottlenose dolphins, and 98 porpoises (P. phocoena) from the UK were 2.3–84, 11 and 119, and 0.12–90 mg kg1 wet weight respectively (Law, 1994). It seems therefore that small cetaceans from the Queensland coast are relatively lightly contaminated with CBs when compared with animals from the UK. Principal component analysis of the CB data demonstrated that the major influence on the first component, accounting for 95% of the variability in the data, stemmed from CB138, CB153 and CB180, which are recalcitrant congeners and those normally accumulated to highest concentration. This primarily reflects quantitative differences in concentrations between CBs in the adult bottlenose dolphin and the other animals. The second component was driven primarily by the concentrations of CB118. This difference was investigated further by normalising the CB concentrations in each case to CB153 (generally the most abundant congener) and repeating the statistical analysis. In this case the first component explained some 97% of the variation in relative CB concentrations, and the bottlenose dolphin calf was highlighted as distinct from the other animals as a result of the higher concentrations of some lower chlorinated CBs (CB31, CB44, CB118) observed in the calf. These differences between the relative CB concentrations in the bottlenose dolphin calf (RJM-03) and the other animals may reflect differences in metabolic capacity, as CB118 is a type III congener with vicinal hydrogen atoms in the ortho- and meta-positions in combination with 1 ortho-chlorine atom, and so can be metabolised by many species of marine mammals (Boon et al., 1997). Table 5 shows a comparison of data for selected organochlorine pesticides and CBs, expressed on a lipid basis, for bottlenose dolphins both from this study and from that of Vetter et al. (2001). The lowest concentrations are observed in the calf, and the highest in the two adult males. Adult females show intermediate concentrations as a result of their ability to reduce their body burden by transfer of lipophilic contaminants to their offspring both across the placenta and in milk.
Acknowledgement This work was funded by the Department for Environment, Food and Rural Affairs as part of its programme of marine environmental research.
References P Aguilar, A., 1984. Relationship of DDE/ DDT in marine mammals to the chronology of DDT input into the ecosystem. Can. J. Fish. Aquat. Sci. 41, 840–844. Allchin, C.R., Kelly, C.A., Portmann, J.E., 1989. Methods of analysis for chlorinated hydrocarbons in marine and other samples. Aquatic Environment Protection: Analytical Method. Ministry of Agriculture, Fisheries and Food, Directorate of Fisheries Research, Lowestoft, (6), 25 pp. Bennett, P.M., Jepson, P.D., Law, R.J., Jones, B.R., Kuiken, T., Baker, J.R., Rogan, E., Kirkwood, J.K., 2001. Exposure to heavy metals and infectious disease mortality in harbour porpoises from England and Wales. Environ. Pollut. 112, 33–40. Bignert, A., Olsson, M., Persson, W., Jensen, S., Zakrisson, S., Litzen, K., Eriksson, U., H€aggberg, L., Alsberg, T., 1998. Temporal trends of organochlorines in Northern Europe, 1967–1995. Relation to global fractionation, leakage from sediments, and international measures. Environ. Pollut. 99, 177–198. Boon, J.P., van der Meer, J., Allchin, C.R., Law, R.J., Klungsyr, J., Leonards, P.E.G., Spliid, H., Storr-Hansen, E., Wells, D.E., McKenzie, C., 1997. Concentration dependent changes of PCB patterns in fish-eating mammals. Structural evidence for induction of cytochrome P450. Arch. Environ. Contam. Toxicol. 33, 298–311. Caurant, F., Amiard-Triquet, C., 1995. Cadmium contamination in pilot whales Globicephala melas: source and potential hazard to the species. Mar. Pollut. Bull. 30, 207–210. de Boer, J., van der Meer, J., 1998. Report on the results of the ICES/ IOC/OSPARCOM intercomparison exercise on the determination of chlorobiphenyl congeners in marine media––steps 3a, 3b, 4 and assessment. ICES Cooperative Research Report, 226. International Council for the Exploration of the Sea, Copenhagen, Denmark. de Boer, J., Wells, D.E., 1997. Chlorobiphenyls and organochlorine pesticides in fish and sediments––Three years of QUASIMEME laboratory performance studies. Mar. Pollut. Bull. 35, 52–63. de Boer, J., Duinker, J.C., Calder, J.A., van der Meer, J., 1992. Interlaboratory study on the analysis of chlorobiphenyl congeners. JAOAC 75, 1054–1062. de Boer, J., van der Meer, J., Reuterg ardh, L., Calder, J.A., 1994. Interlaboratory study on the analysis of chlorobiphenyls in cleaned-up seal blubber and marine sediment extracts. JAOAC 77, 1411–1422. de Swart, R.L., Ross, P.S., Vos, J.G., Osterhaus, A.D.M.E., 1996. Impaired immunity in harbour seals (Phoca vitulina) exposed to
Baseline / Marine Pollution Bulletin 46 (2003) 1200–1211 bioaccumulated environmental contaminants: review of a long-term feeding study. Environ. Health Perspect. 104 (Suppl. 4), 823–828. Dietz, R., Nrgaard, J., Hansen, J.C., 1998. Have Arctic marine mammals adapted to high cadmium levels? Mar. Pollut. Bull. 36, 490–492. Evans, P.G.H., 1987. The Natural History of Whales and Dolphins. Christopher Helm Ltd., Bromley, UK. ISBN 0-7470-0800-0. Jepson, P.D., Bennett, P.M., Allchin, C.R., Law, R.J., Kuiken, T., Baker, J.R., Rogan, E., Kirkwood, J.K., 1999. Investigating potential associations between chronic exposure to polychlorinated biphenyls and infectious disease mortality in harbour porpoises from England and Wales. Sci. Total Environ. 243/244, 339–348. Jones, B.R., Laslett, R.E., 1994. Methods for the analysis of trace metals in marine and other samples. Aquatic Environment Protection: Analytical Method. Ministry of Agriculture, Fisheries and Food, Directorate of Fisheries Research, Lowestoft, (11), 29 pp. Kemper, C., Gibbs, P., Obendorf, D., Marvanek, S., Lenghaus, C., 1994. A review of heavy metal and organochlorine levels in marine mammals in Australia. Sci. Total Environ. 154, 129–139. Law, R.J., 1994. (Compiler). Collaborative UK marine mammal project: summary of data produced 1988–1992. Fisheries Research Technical Report, Ministry of Agriculture, Fisheries and Food, Directorate of Fisheries Research, Lowestoft, (97), 42 pp.
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Law, R.J., 1996. Metals in marine mammals. In: Beyer, W.N., Heinz, G.H., Redmon-Norwood, A.W. (Eds.), Environmental Contaminants in Wildlife: Interpreting Tissue Concentrations. CRC Press, Inc, Boca Raton, USA, pp. 357–376, ISBN 1-56670071-X. Law, R.J., Fileman, C.F., Hopkins, A.D., Baker, J.R., Harwood, J., Jackson, D.B., Kennedy, S., Martin, A.R., Morris, R.J., 1991. Concentrations of trace metals in the livers of marine mammals (seals, porpoises and dolphins) from waters around the British Isles. Mar. Pollut. Bull. 22, 183–191. Law, R.J., Allchin, C.R., Jones, B.R., Jepson, P.D., Baker, J.R., Spurrier, C.J.H., 1997. Metals and organochlorines in tissues of a Blainvilles beaked whale (Mesoplodon densirostris) and a killer whale (Orcinus orca) stranded in the UK. Mar. Pollut. Bull. 34, 208–212. Martin, A.R., 1990. Whales and Dolphins. Salamander Books Ltd., London, ISBN 0-86101-488-X. Vetter, W., Scholz, E., Gaus, C., Muller, J.F., Haynes, D., 2001. Anthropogenic and natural organohalogen compounds in blubber of dolphins and dugongs (Dugong dugon) from northeastern Australia. Arch. Environ. Contam. Toxicol. 41, 221–231. WHO, 1992. Cadmium. Environmental Health Criteria, vol. 134. World Health Organisation, Geneva.
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