Connell, Des

Gaus, Caroline

Haynes, David

Mueller, Jochen

O'Donohue, Mark

Papke, Olaf

University of Queensland eSpace

 
POPS IN MARINE MAMMALS: LEVELS AND EFFECTS  
 
 
EXPOSURE AND POTENTIAL RISKS OF DIOXINS  
TO THE MARINE MAMMAL DUGONG 
 
 
 
Caroline Gaus1, Mark O Donohue2, Des Connell3, Jochen Mueller1, David Haynes4, 
Olaf Paepke5 
 
1University of Queensland, EnTox, Brisbane 
2South East Queensland Water Corporation, Brisbane 
3School of Public Health, Griffith University, Brisbane 
4Great Barrier Reef Marine Park Authority, Townsville 
5Ergo Forschungsgesellschaft mbH, Hamburg 
  
 
 
 
ORGANOHALOGEN COMPOUNDS – Volume 66 (2004) 1559 
Introduction 
 
Atmospheric transport and subsequent deposition is considered a key pathway of PCDD/F input 
into marine systems.  However, their strong affinity for particulates can result in significant 
sediment/soil associated PCDD/F transport from local emissions, in particular within riverine 
systems.  In the subtropical/tropical coastal zone of Queensland, Australia, numerous large-scale 
tributaries feed into shallow embayments of the near shore marine environment.  This environment 
sustains diverse and unique ecosystems associated with the world heritage Great Barrier Reef 
Marine Park.  These include extensive seagrass habitats providing the food source for the only 
strictly herbivorous marine mammal dugong (Dugong dugon).  Dugongs represent the last extant 
species in the family Dugongidae of the order Sirenia (the latter also including three species of 
manatee) and are listed as vulnerable to extinction by the IUCN Red List of Threatened Species.  
While Australia supports the most significant portion of the worlds remaining dugong populations, 
surveys have indicted a strong decline to only 3% of the population estimated in the 1960s1.  
Dugongs frequent coastal waters with habitats predominantly in wide shallow protected bays with a 
relatively small home range, varying from 5 to 64 km2 2.  Dugongs have a long life-span (~70 
years), low reproductive rate and relatively long gestation and lactation periods.  They are hindgut 
fermenters with highly specialized dietary requirements, uprooting whole seagrass plants and often 
selectively foraging on a few pioneer seagrass species3.  Low metabolic rates, high seagrass 
consumption rates and inordinately long passage times of digesta through the gut (~6-7 days)4, 
compensate for the low nutrient containing seagrass diet.  Long life span, high fat repositories, 
narrow home ranges and highly specialized food requirements render the dugong potentially 
vulnerable to the regional PCDD/F contamination observed in Queensland.  The present study 
aimed to establish baseline information for PCDD/F concentrations in dugongs from Queensland, 
to determine the exposure pathways involved and evaluate potential associated risks.   
 
 
 
POPS IN MARINE MAMMALS: LEVELS AND EFFECTS  
 
 
ORGANOHALOGEN COMPOUNDS – Volume 66 (2004) 1560 
Materials and Methods  
 
Blubber tissue from dugongs was obtained from animals found stranded within six 
regions along the coastline of Queensland and one region in the Northern Territory 
(Darwin).  Throughout this paper, the regions in Queensland (Far North, Cairns, 
Hinchinbrook, Whitsundays, Hervey Bay and Moreton Bay), are referred to as 
Region 1 to 6 (respectively).  Blubber samples were taken from the outer layer of 
blubber and together with previously reported data from dugong tissue5, 6 a total of 
7 adult males and 15 adult females were included in results and interpretation for 
this paper.  The tissue was digested using 4 molar HCl at 60 °C and lipid content 
was determined gravimetrically.  All samples were analysed for full PCDD/F 
profiles at ERGO Forschungsgesellschaft mbH in Germany using standardized 
techniques5, 6.   
 
For calculation of average daily intake (ADI), the following parameters have been 
used: (1) Dugong body weight: average 370 kg (320-470 kg) – based on records 
obtained for the animals of this study.  (2) Seagrass consumption: average 35 kg 
wet weight (4 kg dry weight) per day – this is within the range of estimated 
consumption rates2, 4.  (3) Sediment consumption: 2 kg dry weight per day.  No 
information on sediment consumption rate exists, and the estimate was based on 
seagrass:sediment weight ratios determined from samples rinsed thoroughly in 
seawater7.  (4) Total body lipid: average 35% (30-40%) of body weight – no 
records could be obtained for dugongs and the estimate was based on reports from 
other marine mammals.  (5) Steady state conditions were assumed for estimation 
of half-life (T2) using the equation T2=(ln(2)*BDug)/(f*IDug)8, where BDug is the 
body burden of dugongs (ng kg-1), f is the fraction absorbed (%) and IDug is the 
intake (ng kg-1 day-1). 
 
POPS IN MARINE MAMMALS: LEVELS AND EFFECTS  
 
 
ORGANOHALOGEN COMPOUNDS – Volume 66 (2004) 1561 
Results and Discussion  
 
PCDD/Fs were detected in all dugong samples analysed (range ∑PCDD/Fs 225-2000 and 80-1200 
pg g-1 lipid adult males and females, respectively).  While considerable differences were present in 
dugong ∑PCDD/F concentrations from all regions (Coefficient of Variation (CV) = 104 and 79% 
males and females, respectively), variability was relatively low in animals from the same region, in 
particular among adult males (range CV = 2.2-25% and 27-50% males and females, respectively).  
This suggests that the PCDD/F 
exposure of dugongs from 
Queensland is governed by 
localized pathways.  
Differences in dugong 
PCDD/F concentrations 
between Queensland habitat 
regions were previously 
observed from initial data and 
were suggested to be 
correlated to the sediment 
OCDD contamination 
observed in seagrass habitats 
(OCDD sediment screening 
was previously established as a 
reliable proxy for ∑PCDD/F 
contamination in 
Queensland)5.  The additional 
animals analysed for this study 
confirm a significant 
(p<0.0005) linear correlation 
between the ∑PCDD/F 
concentrations in dugongs and average OCDD concentrations in sediments from their habitats 
(Figure 1).  Hence, the relatively simple OCDD screening method may provide a cost-effective 
initial strategy for dugong PCDD/F exposure assessment in Queensland.  In general, PCDD/F body 
burdens of most, higher trophic, marine mammals are influenced by various uptake and transfer 
processes, including complex interactions within the food web, which often also encompass a wide 
spatial extent within the marine system.  In the relatively regionalized, herbivorous dugong, most 
food web processes and large-scale spatial influences are removed.  Hence, the PCDD/F 
concentrations in dugongs reflect the regional PCDD/F contamination of near shore marine 
sediments in Queensland.  Preliminary results from other studies in Queensland suggest that the 
key input pathway for this contamination, in turn, is associated with sediment/soil transport via 
riverine runoff9.  
 
Highest PCDD/F concentrations were observed in adult male dugongs, and within a given region, 
concentrations were on average 3.4-fold lower in adult females (Figure 1).  Lower concentrations 
in adult females, in combination with the higher variability described above in adult female 
compared to adult male dugongs within a region, is most likely due to the females’ potential to 
eliminate PCDD/Fs via gestation and lactation.  Therefore, while the PCDD/F concentrations of 
R2=0.99
0 2500 5000 7500 10000
0
250
500
750
1000
1250
1500
1750
2000
Adult males, n=9
Adult females, n=16
Average sediment OCDD concentration pg g-1 dw
R2=0.90
PC
D
D
/F
 p
g 
g-
1
lip
id
PC
D
D
/F
 p
g 
g-
1
lip
id
Figure 1.  PCDD/F concentrations in adult male and adult female dugongs
compared to the average sediment OCDD concentrations from different
regions along the Queensland coastline.  Error bars represent standard
deviations and 95 percentiles are given above and below the calculated
mean. 
 
POPS IN MARINE MAMMALS: LEVELS AND EFFECTS  
 
 
ORGANOHALOGEN COMPOUNDS – Volume 66 (2004) 1562 
dugongs are a function of habitat contamination, the variation within a region, and importantly the 
slope of the function itself, is a reflection of dugong specific biological and toxicokinetic processes, 
such as PCDD/F absorption, metabolism and reproductive status. 
 
Compared to other mammals, the PCDD/F concentrations in dugongs from most regions in 
Queensland exceed those reported in dugongs from Thailand and higher trophic marine mammals 
from locations remote to or with relatively low industrial activities and population densities such as 
the Arctic10, New Zealand11 and South Australia12.  PCDD/F concentrations in dugongs from the 
highest contaminated Region 5, (average ∑PCDD/Fs 1900 and 718 pg g-1 lipid in adult male and 
females, respectively) exceed those reported in a range of higher trophic adult marine mammals 
near relatively polluted areas such as the Mediterranean, Baltic and Japan, and similar 
concentrations were reported for adult male killer whales off the British Columbian coast13 (1250-
2400 pg g-1 lipid).  While the dugong is mostly removed from potential biomagnifications of lower 
chlorinated, more toxic PCDD/F congeners through the food chain (due to its herbivorous nature), 
and sediment TEQ levels are low (average 1.6, range 0.072-7.0 pg g-1 dw), PCDD/F concentrations 
expressed as TEQ in dugong blubber were surprisingly high (range 5-140 and 0.92-55 pg g-1 lipid 
in adult males and females, respectively) compared to those reported for higher trophic marine 
mammals elsewhere.  Similar to ∑PCDD/F concentrations, TEQ levels in dugongs were highly 
dependant on habitat regions.  However, it should be highlighted that, in contrast to many other 
marine mammals, PCB concentrations analysed from some dugongs in Queensland indicate that 
their contribution to the TEQ are relatively low14. 
 
The PCDD/F congener profiles in all adult animals were dominated by OCDD (average 50% of 
∑PCDD/Fs), followed by 1,2,3,4,6,7,9-HpCDD (average 14%), whereas PCDFs only contributed 
on average 11% to the total ∑PCDD/F concentrations, and most PCDF congeners were present at 
levels below the limit of detection.  In addition to the laterally chlorinated PCDD/Fs, non-2,3,7,8-
substituted PCDD/Fs were present in dugong blubber, with remarkably high contributions within 
each homologue group, in particular the 1,4,6,9-substitued PCDD isomers (e.g. 33% for 
1,2,4,7/1,2,4,8/1,3,7,8/1,4,6,9-TCDD, 8% for 1,2,4,6,9-PnCDD, 2.2% for 1,2,4,6,7,9/1,2,4,6,8,9-
HxCDD) (Figure 2).  Comparing the PCDD/F isomer distributions found in dugongs with those 
found in sediments and seagrass previously reported from near shore environments in Queensland, 
it was apparent that the patterns of non-2,3,7,8-substituted congeners in the animals follow closely 
those observed in sediments (Figure 2) and their food source, seagrass.  While this contrasts the 
almost exclusive accumulation of laterally substituted congeners generally observed in mammals, 
the presence of non-2,3,7,8-substituted PCDD/Fs in dugongs likely represents the overriding 
contribution of these isomers in the food source, in combination with the dugongs low trophic 
position and high seagrass/sediment consumption rates, which may exceed its elimination 
capacities for non-lateral chlorinated PCDD/Fs.  In fact, bioaccumulation factors (dugong to 
sediment plus seagrass concentration ratios) for all non-lateral substituted PCDD isomers were 
considerably lower (<1) compared to the 2,3,7,8-PCDDs (>30 for TCDD and PnCDD, 6-24 for 
HxCDDs, and 3 for HpCDD;  (0.2 for OCDD)).   
 
POPS IN MARINE MAMMALS: LEVELS AND EFFECTS  
 
 
ORGANOHALOGEN COMPOUNDS – Volume 66 (2004) 1563 
 
0
10
20
30
40
50
60
70
80
90
100
Sediment
Dugong
 
Figure 2.  PCDD isomer distributions (% concentration of ∑homologue concentration) in a representative sediment 
and dugong blubber sample from Queensland. 
 
The results of the present study suggest that exposure to PCDD/Fs by dugongs is related to the 
local contaminant concentrations in their inshore habitats, which in turn may be governed by 
terrestrial runoff and sediment transport within river plumes in Queensland9.  Accumulation of 
sediment-bound PCDD/Fs in the near-shore coastal zone leads to elevated concentrations in the 
sediment-seagrass system.  From sediments and seagrass, PCDD/Fs are redistributed to dugongs 
via preferred bioaccumulation (and selective transfer to offspring, unpublished data) of 
toxicological relevant PCDD/Fs.  These results, together with laboratory and field evidence 
implicating toxic effects at relatively low levels in mammals, may represent risks for existing and 
future dugong populations.  The results from the present study have been used to semi-quantify 
such risks.  To accurately quantify risks, however, the sensitivity in dugongs would have to be 
determined.  As these data are not available to date, it is highlighted that the following presents an 
estimate of potential risks in comparison to sensitive biological endpoints observed in other 
mammals. 
 
Although the toxic effects of PCDD/Fs act over a common mediator (binding to the Ah-receptor), 
there are considerable species-specific differences in the responses elicited by these compounds15.  
In light of the unknown susceptibility of dugongs to PCDD/Fs, however, a conservative approach 
would be to expect that the endpoints for dugongs are at least comparable to those determined for 
experimental animals with respect to adverse health effects.  Lowest dose (LOAELs), at which 
statistical significant effects on most sensitive endpoints were observed in mammals, have resulted 
in TEQ body burdens of 28 to 73 ng kg-1.  These effects include neurotoxic, reproductive, 
 
POPS IN MARINE MAMMALS: LEVELS AND EFFECTS  
 
 
ORGANOHALOGEN COMPOUNDS – Volume 66 (2004) 1564 
endocrine and immunotoxic responses8.  Biochemical endpoints, observed at body burdens as low 
as 3 ng kg-1, were not included in this assessment.  
 
Average daily TEQ intake (ADI) of adult dugongs (calculated using the equation presented in 
materials and methods) was estimated at 3.1, 104, 42, 17, 170 and 15 pg kg-1 in the region 1 to six, 
respectively.  These exposure levels resulted in average body burdens of 11, 3.1 and 47 ng kg-1 in 
adult males from region 3, 4 and 5, and 1,3, 4,0 and 1.5 ng kg-1 in adult females from region 1,2 
and 6, respectively.  Using the above LOAELs determined for other mammals (28-72 ng kg-1), and 
average daily intake and body burdens determined for the present study, the PCDD/F intake rate, at 
which adverse effects may occur in dugongs are in the range of 104 to 270 pg kg-1 day-1.  Since 
the LOAELs are based on experimental animals, an uncertainty factor of 10 is commonly used to 
account for species differences in toxicokinetics.  By applying the same uncertainty for dugongs, a 
TDI of 10 to 27 pg kg-1 day-1 was calculated.  Dugongs from regions 2,3,and 5 exceed this TDI by 
3.9-10, 1.6-4.2 and 6.3-17 fold, respectively. 
 
 
In order to provide an 
initial quantitative 
estimate of the risks to 
the dugong population 
of Queensland from 
exposure to PCDD/Fs, 
the probabilistic 
distribution of TEQ 
body burdens in adult 
dugongs (including 
males and females) was 
calculated.  The 
calculation was based 
on the lognormal 
distributions of lipid 
TEQ concentrations and 
body weight observed 
for this study as well as an assumed lognormal distribution of body lipid content.  The output 
distribution of TEQ body burden in dugongs is presented in Figure 3.  Assuming that the data 
obtained for this study is representative for the dugong population of Queensland, and compared to 
the LOAELs above, up to 1.6-21% of the population are at or above the range of levels (LOAEL) 
where physiological effects have been observed in other mammals.  It has to be noted, however, 
that this assessment is compromised by the lack of information on dugong specific sensitivities to 
dioxin-like compounds and actual risks may be lower (or higher).  Nevertheless, the relatively high 
PCDD/F contamination of the dugongs’ food source, its high seagrass consumption rates, preferred 
retention of toxicologically more relevant congeners, low elimination/high bioavailability and 
selective transfer to offspring, highlight the need for a detailed investigation of the sensitivity of 
dugongs to PCDD/Fs.  This is of particular interest, since dugongs, due to their near shore habitats, 
are exposed to numerous other anthropogenic pressures, and an excess mortality of only 5% is 
considered unsustainable for these populations16. 
Figure 3.  Probabilistic distribution of body burdens in the dugong population of
Queensland.  The blue area indicates the fraction of the population at or above the
LOAEL of 10 pg/kg (immunotoxicity) observed in other mammals.  
Cumulative Chart
Certainty is 20.92% from 10.00 to +Infinity ng/kg body weight
.000
.250
.500
.750
1.000
0
10000
0.01 15.91 31.81 47.70 63.60
10,000 Trials    161 Outliers
Forecast: Dugong TEQ body burden (ng/kg)
 
POPS IN MARINE MAMMALS: LEVELS AND EFFECTS  
 
 
ORGANOHALOGEN COMPOUNDS – Volume 66 (2004) 1565 
 
Acknowledgements 
This project was funded by the Australian Research Council with partner contributions from Ergo 
Forschungsgesellschaft, the Great Barrier Reef Marine Park Authority and Queesland Health 
Scientific Services.  The collection of dugong samples would not have been possible without access 
to the stranding network provided and maintained by Queensland Parks and Wildlife Services and 
the Great Barrier Reef Marine Park Authority.  EnTox is co-funded by Queensland Health 
Scientific Services.   
 
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POPS IN MARINE MAMMALS: LEVELS AND EFFECTS  
 
 
ORGANOHALOGEN COMPOUNDS – Volume 66 (2004) 1566 
 


Exposure and potential risks of dioxins to the marine mammal dugong

http://espace.library.uq.edu.au/view/UQ:101207/P475.pdf

Exposure and potential risks of dioxins to the marine mammal dugong

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