9
Organochlorine and heavy metal concentrations in blubber and liver tissue collected from Queensland (Australia) dugong (Dugong dugon) David Haynes a, * , Steve Carter b , Caroline Gaus c , Jochen Mu ¨ ller c , William Dennison d,1 a Great Barrier Reef Marine Park Authority, P.O. Box 1379, Townsville 4810, Australia b Queensland Health and Scientific Services, P.O. Box 594, Archerfield 4108, Australia c National Research Centre for Environmental Toxicology, The University of Queensland, 39 Kessels Rd, Coopers Plains 4121, Australia d Marine Botany, The University of Queensland, St. Lucia 4072, Australia Abstract Tissue samples of liver and blubber were salvaged from fifty-three dugong (Dugong dugon) carcasses stranded along the Queens- land coast between 1996 and 2000. Liver tissue was analysed for a range of heavy metals and blubber samples were analysed for organochlorine compounds. Metal concentrations were similar in male and female animals and were generally highest in mature animals. Liver concentrations of arsenic, chromium, iron, lead, manganese, mercury and nickel in a number of individual animals were elevated in comparison to concentrations previously reported in Australian dugong. Dieldrin, DDT (and its breakdown prod- ucts) and/or heptachlor epoxide were detected in 59% of dugong blubber samples. In general, concentrations of organochlorines were similar to those reported in dugong 20 years earlier, and were low in comparison to concentrations recorded from marine mam- mal tissue collected elsewhere in the world. With the exception of lead, the extent of carcass decomposition, the presence of disease or evidence of animal starvation prior to death did not significantly affect dugong tissue concentrations of metals or organochlo- rines. The results of the study suggest that bioaccumulation of metals and organochlorine compounds (other than dioxins) does not represent a significant risk to Great Barrier Reef dugong populations, particularly in the context of other pressures associated with coastal development and other anthropogenic activities. Ó 2004 Elsevier Ltd. All rights reserved. Keywords: Bioaccumulation; Dioxins; Dugongs; Great Barrier Reef; Heavy metals; Marine mammals; Organochlorines; Seagrass 1. Introduction Southern Great Barrier Reef (Australia) dugong (Du- gong dugon) populations are documented to have under- gone a massive decline over the last 40 years (Marsh et al., 1994, 1995, 2001). This is of particular concern as populations of this herbivorous marine mammal are threatened or in decline throughout much of its world- wide range (Marsh et al., 1999). Although large popula- tions of dugong still exist, principally in Australian waters (Preen, 1993), the species is considered to be vul- nerable to extinction (IUCN, 1996). Definitive reasons for the species decline are unclear, but are likely to in- clude legal and illegal hunting, boat strikes and acciden- tal capture in fishing nets, as well as loss of seagrass habitat and the release of pollutants following coastal and hinterland development (Haynes et al., 1998; Marsh et al., 1999). Recent surveys of pollutant concentrations in Great Barrier Reef habitat have indicated that near- shore marine sediments contain a range of organochlo- rine pollutants including DDT and its breakdown 0025-326X/$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2004.10.020 * Corresponding author. Tel.: +61 7 47500700; fax: +61 7 47726093. E-mail address: [email protected] (D. Haynes). 1 Present address: University of Maryland, College Park, MD 20742, USA. www.elsevier.com/locate/marpolbul Marine Pollution Bulletin 51 (2005) 361–369

Organochlorine and heavy metal concentrations in blubber and liver tissue collected from Queensland (Australia) dugong (Dugong dugon)

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Page 1: Organochlorine and heavy metal concentrations in blubber and liver tissue collected from Queensland (Australia) dugong (Dugong dugon)

www.elsevier.com/locate/marpolbul

Marine Pollution Bulletin 51 (2005) 361–369

Organochlorine and heavy metal concentrations in blubberand liver tissue collected from Queensland (Australia)

dugong (Dugong dugon)

David Haynes a,*, Steve Carter b, Caroline Gaus c, Jochen Muller c, William Dennison d,1

a Great Barrier Reef Marine Park Authority, P.O. Box 1379, Townsville 4810, Australiab Queensland Health and Scientific Services, P.O. Box 594, Archerfield 4108, Australia

c National Research Centre for Environmental Toxicology, The University of Queensland, 39 Kessels Rd, Coopers Plains 4121, Australiad Marine Botany, The University of Queensland, St. Lucia 4072, Australia

Abstract

Tissue samples of liver and blubber were salvaged from fifty-three dugong (Dugong dugon) carcasses stranded along the Queens-

land coast between 1996 and 2000. Liver tissue was analysed for a range of heavy metals and blubber samples were analysed for

organochlorine compounds. Metal concentrations were similar in male and female animals and were generally highest in mature

animals. Liver concentrations of arsenic, chromium, iron, lead, manganese, mercury and nickel in a number of individual animals

were elevated in comparison to concentrations previously reported in Australian dugong. Dieldrin, DDT (and its breakdown prod-

ucts) and/or heptachlor epoxide were detected in 59% of dugong blubber samples. In general, concentrations of organochlorines

were similar to those reported in dugong 20 years earlier, and were low in comparison to concentrations recorded from marine mam-

mal tissue collected elsewhere in the world. With the exception of lead, the extent of carcass decomposition, the presence of disease

or evidence of animal starvation prior to death did not significantly affect dugong tissue concentrations of metals or organochlo-

rines. The results of the study suggest that bioaccumulation of metals and organochlorine compounds (other than dioxins) does

not represent a significant risk to Great Barrier Reef dugong populations, particularly in the context of other pressures associated

with coastal development and other anthropogenic activities.

� 2004 Elsevier Ltd. All rights reserved.

Keywords: Bioaccumulation; Dioxins; Dugongs; Great Barrier Reef; Heavy metals; Marine mammals; Organochlorines; Seagrass

1. Introduction

Southern Great Barrier Reef (Australia) dugong (Du-

gong dugon) populations are documented to have under-

gone a massive decline over the last 40 years (Marshet al., 1994, 1995, 2001). This is of particular concern

as populations of this herbivorous marine mammal are

threatened or in decline throughout much of its world-

0025-326X/$ - see front matter � 2004 Elsevier Ltd. All rights reserved.

doi:10.1016/j.marpolbul.2004.10.020

* Corresponding author. Tel.: +61 7 47500700; fax: +61 7 47726093.

E-mail address: [email protected] (D. Haynes).1 Present address: University of Maryland, College Park, MD

20742, USA.

wide range (Marsh et al., 1999). Although large popula-

tions of dugong still exist, principally in Australian

waters (Preen, 1993), the species is considered to be vul-

nerable to extinction (IUCN, 1996). Definitive reasons

for the species decline are unclear, but are likely to in-clude legal and illegal hunting, boat strikes and acciden-

tal capture in fishing nets, as well as loss of seagrass

habitat and the release of pollutants following coastal

and hinterland development (Haynes et al., 1998; Marsh

et al., 1999). Recent surveys of pollutant concentrations

in Great Barrier Reef habitat have indicated that near-

shore marine sediments contain a range of organochlo-

rine pollutants including DDT and its breakdown

Page 2: Organochlorine and heavy metal concentrations in blubber and liver tissue collected from Queensland (Australia) dugong (Dugong dugon)

362 D. Haynes et al. / Marine Pollution Bulletin 51 (2005) 361–369

products as well as dieldrin and lindane and PCDD/Fs

(Muller et al., 1999; Haynes et al., 2000a; Gaus, 2002).

Accumulation of organochlorine pesticides and poly-

chlorinated biphenyls (PCBs) has been implicated in

reproductive, nervous system and immunological abnor-

malities observed in marine mammal populations in theNorthern Hemisphere (Reijnders, 1986; Brouwer et al.,

1989; Kuiken et al., 1994; de Swart et al., 1996; Johnston

et al., 1996). Examples include adrenocortical hyperpla-

sia and disruption of steroid metabolism in seals attrib-

uted to DDE metabolites (methylsulphones) produced

in the liver (Lund, 1994), and reduced testosterone con-

centrations in Dall�s porpoise (Phocoenidae dalli) caused

by organochlorine contamination (Subramanian et al.,1987). The consequences of accumulation of elevated

heavy metals in marine mammals is less clear (Langston,

1990; O�Shea, 1999).Most studies of environmental contaminants in mar-

ine mammals have been based on the determination of

residues of organochlorine compounds and metals in

small cetaceans and pinnipeds (O�Shea and Brownell,

1994). Little is known about the accumulation of persis-tent organic pollutants in herbivorous marine mammals

(O�Shea and Brownell, 1994), and very few data exist on

concentrations of heavy metals or organochlorines in

dugong (Heinsohn and Marsh, 1978; Miyazaki et al.,

1979; Denton et al., 1980; Denton, 1981; Vetter et al.,

2001) or the closely related manatee (Trichechus manatus

latirostris) (Forrester et al., 1975; O�Shea et al., 1984;

Ames and van Vleet, 1996). As a consequence, the con-centrations of heavy metals and organochlorine residues

in Queensland dugong and the potential risk they pose

to dugong health in tropical and subtropical Australian

waters remains essentially unknown. This study presents

contemporary data on concentrations of heavy metals

and organochlorines in dugong stranded along the

Queensland coastline between 1996 and 2000 and dis-

cusses potential risks from past exposure of Queenslanddugong to these pollutants.

2. Materials and methods

2.1. Tissue collection

Tissue samples were collected from 53 dugong car-casses stranded on Queensland beaches between Hervey

Bay and Cairns (1200km) from August 1996 to April

2000 (Fig. 1). Twenty four of the carcasses were in good

condition (fresh) at the time of sampling. Twenty-three

animals were in fair condition (decomposing, organs in-

tact), and six sampled animals were in poor condition

(advanced decomposition) at the time of sampling.

The cause of death was unable to be ascertained for26 of the stranded carcasses. Of the others, death re-

sulted from net or mooring entanglement drownings

(n = 7), a suspected underwater explosion (n = 1), star-

vation, with underlying cause unknown, (n = 10), and

pneumonia or infection following wounding (n = 9).

Twenty-eight animals were considered mature (>2.2m

in length; 14 male, 14 female) and 25 animals were

immature (<2.2m in length; 14 male, 10 female, 1 un-known). Samples of blubber and/or liver were collected

from each carcass using standard techniques (Geraci

and Lounsbury, 1993; Eros et al., 2000). Blubber tissue

was collected from the outermost layers of blubber and

muscle, just to one side of the mid-ventral line. Samples

of liver were collected from the left caudal tip of the

organ.

Samples were collected under Scientific Purposes Per-mit No. 0011221/96/SAB, Queensland Nature Conserva-

tion Act 1992. Basic anatomical data were recorded for

each carcass at the time of sampling. Collected tissue

was divided and stored frozen in acid-washed plastic

containers for metal analyses and in solvent-washed

glass containers for organochlorine analyses. Additional

tissue samples were collected for polychlorinated-p-

dibenzodioxin and dibenzofuran (PCDD/F) analysesand for PCB and natural organohalogen compound

analyses, the results of which are reported elsewhere

(Haynes et al., 1999; Vetter et al., 2001; Gaus et al.,

2001; Gaus, 2002).

3. Sample analyses: metals

Tissue metal analyses were carried out by the Re-

sources Sciences Laboratories, Department of Natural

Resources, (Brisbane). Liver samples for metals analyses

were freeze-dried and ground to a fine powder. Approx-

imately 100mg of each dried sample was microwave di-

gested for 16min in double-distilled nitric acid. The

sample was then cooled in an ice bath and the sample

solution made up to 10g with polished reverse-osmosiswater. Three grams of each solution was reserved for

mercury analysis and the remainder (7g) evaporated to

near dryness on a hotplate and a further 2ml of

HNO3 and 2ml of H2O2 was then added drop-wise to

each residue to complete tissue digestion. The digestion

solutions were washed into separate polypropylene

tubes with 1% HNO3, and made up to 20g. Inductively

coupled mass spectrometry (ICP-MS) using a Perkin-El-mer Sciex ELAN 5000 was used to determine sample

solution concentrations of all metals (aluminium, ar-

senic, cadmium, chromium, copper, iron, lead, manga-

nese, mercury, nickel, selenium and zinc).

4. Sample analyses: organochlorines

Tissue organochlorine concentrations were deter-

mined at Queensland Health and Scientific Services Lab-

Page 3: Organochlorine and heavy metal concentrations in blubber and liver tissue collected from Queensland (Australia) dugong (Dugong dugon)

NN

0 100 200 300 400

Kilometres

Q U E E N S L A N D

PAPUAN EW

GUINEA

C O R A L S E A

BRISBANE

Bundaberg

GladstoneRockhampton

Mackay

Ingham

Townsville

Cairns

Ayr

Yeppoon

Proserpine

Bowen

Innisfail

Tully

Port Douglas

LockhartRiver

Port Moresby

Hervey Bay

Nambour

Cooktown

15°S

10°S

145°E 150°E

145°E 150°E

20°S

25°S

10°S

15°S

20°S

25°S

Tropic of Capricorn (23°26.5’S)

BRA Q201 1998

17°30'S147°00'E

10°41'S145°00'E

13°00'S145°00'E

15°00'S146°00'E

21°00'S152°55'E

24°30'S154°00'E

FAR NORTHERNSECTION(Area: 85 050 sq km)

CAIRNS SECTION(Area: 35 500 sq km)

CENTRAL SECTION(Area: 75 850 sq km)

MACKAY / CAPRICORNSECTION

(Area: 143 000 sq km)

GUMOO WOOJABUDDEESECTION

(Area: 350 sq km)

Bamaga

Thursday Island

1

1

1

10

34

7

14

9

3

3

C a r c a s s r e c o v e r y s i t e a n d n u m b e r o f s a m p l e s c o l l e c t e d

Fig. 1. Dugong carcass recovery locations, Queensland, 1996–2000.

D. Haynes et al. / Marine Pollution Bulletin 51 (2005) 361–369 363

oratories (Brisbane). Between 2 and 5g of blubber sam-ple for organochlorine analyses were extracted by mac-

erating the sample in 100ml of acetone in a blender.

The samples were then centrifuged and the supernatant

transferred into separating funnels. This was repeated

twice and the extracts were combined. A 100ml aliquot

of dichloromethane (DCM) and 5ml of saturated NaCl

aqueous solution were added to the supernatant. Fol-

lowing phase separation, the non-polar fraction wasconcentrated, and then passed through a gel-permeation

column (GPC, Envirogel, Waters) using DCM as themobile phase. Following the GPC step, the extract was

taken up in hexane and transferred to a column packed

with 10g of 5% deactivated Florisil. This was eluted with

150ml of 6% diethylether (DEE) in hexane and 100ml of

10% acetone in hexane. The volumes of the individual

fractions were then reduced to 1ml. The samples were

then analysed for HCB (Limit of detection (LOD)

0.1lgkg�1), lindane (LOD 0.2lgkg�1), heptachlor(LOD 0.2lgkg�1), heptachlor epoxide (LOD

Page 4: Organochlorine and heavy metal concentrations in blubber and liver tissue collected from Queensland (Australia) dugong (Dugong dugon)

Table 2

Recoveries (%) of organochlorine compounds in spiked samples

Compound c7–c13 c17–c19 c23–c26 c27–c52 c53–c98

HCB 64 18 35 71 88

Lindane 89 41 61 98 123

Heptachlor 91 32 56 72 134

364 D. Haynes et al. / Marine Pollution Bulletin 51 (2005) 361–369

0.2lgkg�1), aldrin (LOD 0.2lgkg�1), dieldrin (LOD

0.2lgkg�1), DDT (LOD 0.2lgkg�1), DDE (LOD

0.1lgkg�1) and DDD (LOD 0.2lgkg�1) on a gas chro-

matograph employing an electron capture detector

(GC-ECD). The total lipid content of each sample was

determined gravimetrically.

Heptachlor epoxide 96 na 62 93 110

Dieldrin 101 34 48 102 106

Aldrin 84 22 31 87 112

DDT (pp) 115 52 80 98 112

DDE (pp) 102 44 67 98 132

DDD (pp) 104 46 78 93 108

PCBs na na na 84 na

na: not available.

5. Quality assurance and statistical analysis

Certified Standard Reference Material (National Re-

search Council, Canada; DORM-2; dogfish muscle), re-

agent blanks and sample duplicates were analysed

concurrently with dugong tissue to validate the metalanalyses methods used (Table 1). Reagent blanks and

spiked recovery samples for organochlorine compounds

were analysed concurrently with dugong tissue samples.

Average recoveries of spikes ranged from 18% to 115%

(Table 2). No organochlorines were detected in reagent

blanks.

Three-way analysis of variance (ANOVA; a = 0.05)

was used to compare dugong liver metal concentrationsand animal maturity (juvenile or adult), gender and

health status (healthy, unhealthy or unknown condition)

using animal body condition (good, fair, poor) as an

analysis covariate (Borrell and Aguilar, 1990). Un-

healthy animals were those that showed evidence of star-

vation or disease at autopsy. Data were plotted and

visually assessed for gross deviations from normality

and, where necessary, transformed (log10) prior to anal-yses. Where metal concentrations were less than detec-

tion limits, values were assigned at half the detection

limit. Two-way ANOVA (a = 0.05) was used to investi-

gate the relationship between detectable blubber orga-

nochlorine concentrations (DDE and dieldrin) and

animal maturity and health status (healthy, unhealthy,

unknown) using animal body condition (good, fair,

poor) as an analysis covariate (Borrell and Aguilar,

Table 1

Average recoveries (%) of Standard Reference Material (DORM 2, Dogfish

Metal Average recovery,

samples 1996

Average recovery,

samples 1997

Average re

samples 19

Al 88 83 91

As 106 87 88

Cd 100 100 100

Cr 87 80 96

Cu 98 101 88

Fe na 91 105

Pb 109 115 123

Mn 93 86 100

Hg 97 95 96

Ni 91 81 99

Se 109 86 81

Zn 95 86 96

na: not available.

1990). Statistical analyses were performed using the

SYSTAT V7.0 statistical package (Wilkinson, 1996).

6. Results

6.1. Metals

Thirty-eight liver tissue samples were collected from

stranded dugong carcasses and analysed for metal con-

centrations between 1996 and 2000. Detectable concen-

trations of all metals analysed were present in dugong

liver, although not all dugongs had detectable concen-

trations of all metals (Table 3). Average concentrations

of all metals were similar to those reported in dugong

previously, although elevated concentrations of one ormore of arsenic, chromium, iron, mercury, manganese,

nickel and/or lead were present in individual animals

collected from the wet tropics region (Cairns to Towns-

ville), the central Queensland coast (the Whitsundays)

and/or Hervey Bay (southern Queensland coast). The

generally higher concentrations of metals present in du-

gong stranded in the vicinity of Hervey Bay may have, in

part, been sourced from the urban environment of Mor-

muscle, National Research Council, Canada)

covery,

98

Average recovery,

samples 1999

Average recovery,

samples 2000

86 75

77 92

105 110

88 84

107 90

108 99

94 na

99 84

94 104

84 73

91 95

104 86

Page 5: Organochlorine and heavy metal concentrations in blubber and liver tissue collected from Queensland (Australia) dugong (Dugong dugon)

Table 3

Summary statistics, dugong liver metal concentrations (all concentra-

tions, mgkg�1 wet weight)

Mature animals (n = 18) Minimum Maximum Mean SD

Length (cm) 213 320 263 31

% Tissue wet weight 69 80 75 4

Al <5 157

As 0.45 7.7 3.0 1.9

Cd <0.005 32.5

Cr 0.2 18 2.7 4.0

Cu 9.5 303 101 89

Fe 1660 172,300 35,776 48,321

Hg 0.05 1.11 0.3 0.29

Pb <0.08 3.08

Mn <1 35

Ni <0.16 14

Se <0.02 3.6

Zn 458 5375 2658 1400

Immature animals (n = 20)

Length (cm) 110 205 154 26

% Tissue wet weight 69 85 77 3

Al <5 264

As 0.04 5.3 2.1 1.6

Cd <0.005 3.0

Cr <0.2 10.2

Cu 6.8 259 83 74

Fe 537 12,127 4114 3328

Hg 0.04 0.28 0.09 0.06

Pb <0.08 0.85

Mn <1 33

Ni <0.3 7.4

Se <0.02 2.9

Zn 46 1601 695 400

D. Haynes et al. / Marine Pollution Bulletin 51 (2005) 361–369 365

eton Bay (Brisbane, southern Queensland; Fig. 1) as ani-

mals have been observed to migrate between the two re-

gions to feed. No significant differences between male

and female animals in liver metal concentrations were

detectable (Table 4). Concentrations of aluminium, cad-

mium, iron, lead, mercury and zinc were significantly

higher in the liver of mature animals (Table 4). In con-trast, liver tissue concentrations of manganese were sig-

nificantly higher in immature animals (Table 4). The

general trend of increasing average metal concentrations

with animal maturity in these samples is in accordance

with metal accumulation patterns present in other mar-

ine mammals (Aguilar et al., 1998; O�Shea, 1999; O�Shea

Table 4

Summary (p values) of three-way ANOVAs of dugong liver metal concentra

body condition as an analysis covariate (all metal concentrations dry wt. an

Al As Cd Cr Cu

Maturity 0.05 0.054 <0.001 0.789 0.886

Health 0.068 0.938 0.634 0.060 0.138

Gender 0.927 0.815 0.995 0.303 0.542

Maturity · health 0.758 0.447 0.205 0.280 0.697

Maturity · gender 0.565 0.992 0.256 0.054 0.513

Health · gender 0.558 0.185 0.345 0.769 0.345

Maturity · health · gender 0.728 0.845 0.443 0.362 0.551

Condition index 0.481 0.967 0.493 0.695 0.407

et al., 1999). Animal health at the time of death (as

determined at autopsy) was not significantly related to

tissue metal concentrations. Tissue lead concentrations

were significantly higher in carcasses in later stages

of carcass decomposition at the time of liver sampling

(Table 4).

7. Organochlorines

Fifty-two blubber samples collected from stranded

dugong between 1996 and 2000 were analysed for orga-

nochlorine concentrations. The concentration of one or

more organochlorine compounds of interest (dieldrin,heptachlor epoxide, DDT, DDD and/or DDE) exceeded

the limit of detection in 30 samples (i.e. 59% of those

analysed). Detectable concentrations of dieldrin, DDT

and DDE ranged from 0.4 to 9.2lgkg�1 wet weight

(1–43lgkg�1 lipid weight), 0.5–59lgkg�1 wet weight

(2.8–66lgkg�1 lipid weight) and 0.3–15.0lgkg�1 wet

weight (0.9–52lgkg�1 lipid weight), respectively. One

blubber sample contained detectable concentrations ofheptachlor epoxide (0.2lgkg�1 wet weight; 0.26lgkg�1

lipid weight) and one blubber sample contained detect-

able concentrations of DDD (6lgkg�1 wet weight;

6.73lgkg�1 lipid weight). Lindane (detection limit

0.1lgkg�1), heptachlor (detection limit 1.0lgkg�1), al-

drin (detection limit 0.2lgkg�1) and HCB (detection

limit 0.1lgkg�1) were not detected in any of the sam-

pled tissues in this study.Average detectable concentrations of DDE expressed

on a lipid weight basis in blubber decreased with increas-

ing age in both male and female animals (Fig. 2)

although these differences were not statistically signifi-

cant (Table 5). Average detectable lipid weight concen-

trations of dieldrin in blubber increased with

increasing maturity in female animals and decreased

with maturity in male animals (Fig. 2), although again,these differences were not statistically significant. Ani-

mal health at the time of death (as determined at au-

topsy) or stage of carcass decomposition at the time of

liver sampling had no significant effect on tissue organo-

chlorine concentration (Table 5).

tions between animals of different age, gender and health status using

d log10 transformed prior to analyses)

Fe Pb Mn Hg Ni Se Zn

<0.001 0.010 0.002 0.007 0.664 0.152 <0.001

0.319 0.159 0.721 0.138 0.120 0.816 0.771

0.993 0.701 0.824 0.758 0.835 0.327 0.521

0.093 0.754 0.094 0.001 0.336 0.627 0.246

0.375 0.762 0.762 0.031 0.188 0.251 0.213

0.002 0.002 0.557 0.538 0.483 0.507 0.696

0.146 0.077 0.187 0.468 0.260 0.305 0.567

0.102 0.028 0.762 0.239 0.470 0.158 0.955

Page 6: Organochlorine and heavy metal concentrations in blubber and liver tissue collected from Queensland (Australia) dugong (Dugong dugon)

Fig. 2. Variability in detectable dugong blubber DDE and dieldrin concentrations (error bars = 1 SEM).

Table 5

Summary (p values) of two-way ANOVA of dugong blubber DDE and

dieldrin concentrations (all concentrations, lgkg�1 lipid weight and

data Log10 transformed prior to analysis)

DDE df Mean square F-ratio p

Maturity 1 0.078 0.215 0.646

Health 2 0.386 1.061 0.356

Maturity · health 2 0.297 0.815 0.450

Body condition 1 0.306 0.841 0.365

Error 41 0.364

Dieldrin

Maturity 1 0.012 0.031 0.861

Health 2 0.616 1.561 0.222

Maturity · health 2 0.015 0.039 0.962

Body condition 1 1.209 3.061 0.088

Error 41

366 D. Haynes et al. / Marine Pollution Bulletin 51 (2005) 361–369

Detectable DDE concentrations varied between sam-

pling regions with highest average concentrations pres-

ent in dugong blubber collected from mature animals

stranded at northern sampling sites between Inghamand the Whitsundays (central Great Barrier Reef coast)

CairnsCardwell

Ingham

TownsvilleBowen

WhitsundaysMackay

Gladstone

Mon Repos

Hervey Bay

Sampling region

0

10

20

30

40

50

60

DD

E (u

g kg

lipi

d w

t)

Fig. 3. Detectable DDE and dieldrin concentrations in Queensland du

and in animals collected from a sampling site further

south at Hervey Bay (Fig. 3). Highest detectable dieldrin

concentrations were present in animals stranded at sam-

pling sites at Cardwell, the Whitsundays and at Hervey

Bay (Fig. 3).

8. Discussion

Concern about the conservation and protection of

marine mammals inevitably extends to considerationof the impact of contaminants (O�Shea et al., 1999).

Dugongs are coastal residents and it is these waters that

tend to receive highest concentrations of metals and or-

ganic pollutants from riverine inflows and direct emis-

sions, as well as the highest rates of atmospheric

pollutant deposition due to their proximity to land-

based sources (Wania et al., 1998). In Queensland, ele-

vated concentrations of a number of heavy metalsderived from igneous parent material are also present

in coastal Queensland sediments (Moss and Costanzo,

1998). Pesticides such as dieldrin and DDT are still

widely distributed in Queensland agricultural soils (Cav-

CairnsCardwell

Ingham

TownsvilleBowen

WhitsundaysMackay

Gladstone

Mon Repos

Hervey Bay

Sampling region

0

10

20

30

40

50

Die

ldrin

(ug

kg li

pid

wt)

gong blubber by carcass salvage location (error bars = 1 SEM).

Page 7: Organochlorine and heavy metal concentrations in blubber and liver tissue collected from Queensland (Australia) dugong (Dugong dugon)

Table 6

Comparison of metal concentrations in Australian dugong liver tissue (all metal concentrations, mgkg�1 dry weight)

Location Northern Australia

Dugonga (Denton et al.,

1980; Denton and

Breck, 1981)

McArthur River

Dugong

(Marsh, 1989)

McArthur River

Dugong (Parry and

Munksgaard, 1992, 1993)

Torres Strait Dugongc

(Dight and Gladstone,

1993; Gladstone, 1996)

Torres Strait

Dugong

(Haynes and

Kwan, 2001)

Queensland

Coast Dugong

(this study)

Date 1974–1978 1984 1992–1993 1991–1993 1997–1999 1996–2000

Sample size 43 2 3 3 36 38

Al <4 <5–264

As 0.2–0.8 0.9–1.9 0.26–2 0.04–7.7

Cd <0.1–58.8 16.4–36.6 10–15 23–46 0.44–54 <0.005–32

Cr <0.5 <0.1–2.9 <0.2–18

Cu 9.1–608 22–107 8.6–28 105–1760 823–1795 7–303

Fe 778–82,363 25,879–69,377 462–34,137 540–172,300

Hg 0.24b <0.02–0.03 0.1–0.19 <0.005–0.22 0.04–1.11

Mn 1.3–9.2 4.0–9.9 <0.6–7.0 <1–35

Ni <0.3 <0.16–1.32 <3–14

Pb <0.3 0.17–0.42 0.24–0.48 <0.04 <0.1–3.1

Se 5.2–7.6 0.40–4.2 <0.02–3.6

Zn 219–4183 1378–1928 1002–1448 470–3430 260–1166 46–5375

a Dugongs sampled in Townsville (n = 14), Torres Strait (n = 1), Cairns (n = 1) and Mornington Island (n = 27).b Originally reported as wet wt. (conversion factor = 4.17).c Originally reported as wet wt. (conversion factor = 4.76).

D. Haynes et al. / Marine Pollution Bulletin 51 (2005) 361–369 367

anagh et al., 1999; Muller et al., 2000) and this is re-

flected in their occurrence in nearshore subtidal sedi-

ments along the Queensland wet-tropics coastline

(Haynes et al., 2000a).A number of pollutants were detected in dugong

stranded along the Queensland coast between 1996

and 2000. Concentrations of metals in dugong liver were

generally similar to, or lower than those reported previ-

ously in dugong collected from different regions along

the northern Australian coast and in Torres Strait

(Table 6). Concentrations of dieldrin and DDT and its

metabolite DDE were present in relatively low concen-trations in dugong blubber in this study. Dieldrin con-

centrations were similar to those reported in the liver

of dugong collected from the same region more than

20 years earlier (0.32–1.02lgkg�1 wet weight) (Hein-

sohn and Marsh, 1978).

Dieldrin concentrations were also low compared with

those in marine mammals from elsewhere, including

both baleen and toothed whales (typically <100lgkg�1

and 70–3600lgkg�1 wet weight, respectively) (O�Sheaand Brownell, 1994; Jarman et al., 1996; Law et al.,

1997; Holsbeek et al., 1999). Total DDT concentrations

in dugong blubber were one to three orders of magni-

tude lower than those typically found in other marine

mammals (<5–100gkg�1), including seals (Tanabe et

al., 1994; Oehme et al., 1996; Aguilar et al., 1998), belu-

ga whales (Muir et al., 1996); dolphins (Kannan et al.,1993; Vetter et al., 2001) and baleen whales (de Kock

et al., 1994; O�Shea and Brownell, 1994; Guitart et al.,

1996). Concentrations of RDDT in dugong blubber

were also two orders of magnitude lower than levels de-

tected in liver of Florida manatee (Ames and van Vleet,

1996).

Gender and age patterns of accumulation of detect-

able DDE and dieldrin concentrations (expressed on a

lipid weight basis) in dugong did not follow the general

trend of increased concentrations in mature males com-pared with immature males and a decline in concentra-

tions in females with maturity associated with

maternal contaminant transfer (Aguilar et al., 1998;

O�Shea et al., 1999; O�Shea, 1999). The reason for this

is presently unknown, and may simply be a consequence

of the generally low concentrations of these contami-

nants in the Great Barrier Reef environment. However,

persistent contaminants are generally incorporated intothe body of marine mammals through food intake (Agu-

ilar et al., 1998), and dugong feed by uprooting entire

seagrass plants from the benthos (Spain and Heinsohn,

1973; Preen, 1995). As a consequence, variations in

dugong body burdens of organochlorine residues (and

heavy metal concentrations) could also be related to

variation in sediment and seagrass pollutant concentra-

tions, as well as the reproductive history and age of maleand female animals.

Toxicity of accumulated metals in marine mammals

is related to cellular enzyme inactivation. However, with

the exception of mercury, no experimental or field col-

lected data has yet demonstrated a toxic impact of accu-

mulated metals in marine mammals (Johnston et al.,

1996; O�Shea, 1999). Although cause of death was not

established conclusively for a majority of the Queens-land dugong carcasses, metal concentrations were typi-

cally low compared with concentrations present in

healthy animals killed during traditional hunting

(Haynes and Kwan, 2001). It is therefore unlikely that

heavy metal accumulation and toxicity played a signifi-

cant part in Queensland dugong strandings and/or

Page 8: Organochlorine and heavy metal concentrations in blubber and liver tissue collected from Queensland (Australia) dugong (Dugong dugon)

368 D. Haynes et al. / Marine Pollution Bulletin 51 (2005) 361–369

deaths. Accumulation of dieldrin and DDT in marine

mammals has demonstrated reproductive and endocrine

disruptive effects (Fossi et al., 1999). However, the con-

centrations of these pollutants accumulated by Queens-

land dugong are relatively low compared to those

accumulated in marine mammals elsewhere. It is there-fore also unlikely that these compounds, with the possi-

ble exception of dioxins (Haynes et al., 1999; Gaus,

2002; Gaus et al., 2001) present a significant risk to local

dugong populations. A greater, indirect risk to Queens-

land dugong populations is likely to be presented by the

impact of herbicide residues on their nearshore seagrass

food resource (Haynes et al., 2000b).

Acknowledgements

Grahame Byron, Andrew Griffith, Neil Hicks, Craig

Purdon, David Savage and Mike Short (Queensland

Parks and Wildlife Service), Kirstin Dobbs and Cherie

Recchia (Great Barrier Reef Marine Park Authority)

and Tony Preen (James Cook University) are thankedfor assistance with tissue collection. Metal analyses were

coordinated by Glenn Barry (Queensland Department

of Natural Resources and Mines).

References

Aguilar, A., Borrell, A., Pastor, T., 1998. Biological factors affecting

variability of persistent pollutant levels in cetaceans. Report of the

International Whale Commission (Special issue).

Ames, A.L., van Vleet, E.S., 1996. Organochlorine residues in the

Florida manatee, Trichechus manatus latirostris. Marine Pollution

Bulletin 32, 374–377.

Borrell, A., Aguilar, A., 1990. Loss of organochlorine compounds in

the tissue of decomposing stranded dolphins. Bulletin of Environ-

mental Contamination Toxicology 45, 46–53.

Brouwer, A., Reijnders, P.J.H., Koeman, J.H., 1989. Polychlorinated

biphenyl (PCB) contaminated fish induces vitamin A and thyroid

hormone deficiency in the common seal (Phoca vitulina). Aquatic

Toxicology 15, 99–106.

Cavanagh, J.E., Burns, K.A., Brunskill, G.J., Coventry, R.J., 1999.

Organochlorine pesticide residues in soils and sediments of the

Herbert and Burdekin River Regions, north Queensland—impli-

cations for contamination of the Great Barrier Reef. Marine

Pollution Bulletin 39, 367–375.

de Kock, A.C., Best, P.B., Cockcroft, V., Bosma, C., 1994. Persistent

organochlorine residues in small cetaceans from the east and west

coasts of Southern Africa. The Science of the Total Environment

154, 153–162.

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

bioaccumulated environmental contaminants: a review of a long

term study. Environmental Health Perspectives 104, 823–

828.

Denton, G.R.W., Marsh, H., Heinsohn, G.E., Burden-Jones, C., 1980.

The unusual metal status of the dugong Dugong dugon. Marine

Biology 57, 201–219.

Denton, G.R.W., 1981. The effect of diet on the unusual metal status

of the dugong (Dugong dugon (Muller)). In: Marsh, H. (Ed.), The

dugong. James Cook University, Townsville, Australia. pp. 169–

74.

Denton, G.R.W., Breck, W.G., 1981. Mercury in tropical marine

organisms from north Queensland. Marine Pollution Bulletin 12,

116–121.

Dight, I.J., Gladstone, W., 1993. Trace metal concentrations in

sediments and selected marine biota as indicator organisms and

food items in the diet of torres strait islanders and coastal papuans.

Torres Strait Baseline Study: Pilot Study Final Report, June 1993.

Great Barrier Reef Marine Park Authority, Townsville.

Eros, C., Marsh, H., Bonde, R., O�Shea, T., Beck, C., Recchia, C.,

Dobbs, K., 2000. Procedures for the salvage and necropsy of the

Dugong (Dugong dugon). Great Barrier Reef Marine Park Author-

ity Research Publication No. 64, Great Barrier Reef Marine Park

Authority, Townsville.

Forrester, D.J., White, F.H., Woodard, J.C., Thompson, N.P., 1975.

Intussusception in a Florida manatee. Journal of Wildlife Diseases

11, 566–568.

Fossi, M.X.C., Casini, S., Marsili, L., 1999. Nondestructive biomark-

ers of exposure to endocrine disrupting chemicals in endangered

species of wildlife. Chemosphere 39, 1273–1285.

Gaus, C., 2002. Dioxins in the marine environment. Sources, pathways

and fate of polychlorinated dibenzo-p-dioxins and dibenzofurans in

Queensland, Australia. Unpublished Ph.D. thesis, Griffith Univer-

sity, Australia.

Gaus, C., Papke, O., Blanchard, W., Haynes, W., Connell, D.W.,

Muller, J., 2001. Bioaccumulation and pathways of PCDDs in the

lower trophic marine system. Organohalogen Compounds 52,

95–99.

Geraci, J.R., Lounsbury, V.J., 1993. Marine mammals ashore: a field

guide for strandings. Texas A&M University Sea Grant College

Program.

Gladstone, W., 1996. Trace metals in sediments, indicator organisms

and the traditional seafoods of the Torres Strait. Great Barrier

Reef Marine Park Authority, Townsville.

Guitart, R., Guerrero, X., Silvestre, A.M., Gutierrez, J.M., Mateo, R.,

1996. Organochlorine residues in tissues of striped dolphins affected

by the 1990 Mediterranean epizootic: relationships with the fatty

acid composition. Archives of Environmental Contamination and

Toxicology 30, 79–83.

Haynes, D., Kwan, D., 2001. Trace metal concentrations in the Torres

Strait environment and traditional seafood species, 1997–2000.

Torres Strait Regional Authority, Thursday Island, Queensland,

Australia.

Haynes, D., Muller, J., Carter, S., 2000a. Pesticide and herbicide

residues in sediments and seagrasses from the Great Barrier Reef

World Heritage Area and Queensland coast. Marine Pollution

Bulletin 41, 279–287.

Haynes, D., Ralph, P., Prange, J., Dennison, W., 2000b. The impact of

the herbicide diuron on photosynthesis in three species of tropical

seagrass. Marine Pollution Bulletin 41, 288–293.

Haynes, D., Muller, J.F., McLachlan, M.S., 1999. Polychlorinated

dibenzo-p-dioxins and dibenzofurans in Great Barrier Reef

(Australia) dugongs (Dugong dugon). Chemosphere 38, 255–

262.

Haynes, D., Slater, J., Devlin, M., Makey, K., 1998. Great Barrier

Reef water quality monitoring and dugong protection areas. Reef

Research 8, 10–15.

Heinsohn, G.E., Marsh, H., 1978. Ecology and conservation of the

dugong, Dugong dugon, in Australia. Unpublished Report to the

Australian National Parks and Wildlife Service,

Canberra.

Holsbeek, L., Joiris, C.R., Debacker, V., Ali, I.B., Roose, P., Nellissen,

J., Gobert, S., Bouquegneau, J., Bossicart, M., 1999. Heavy metals,

organochlorines and polycyclic aromatic hydrocarbons in sperm

Page 9: Organochlorine and heavy metal concentrations in blubber and liver tissue collected from Queensland (Australia) dugong (Dugong dugon)

D. Haynes et al. / Marine Pollution Bulletin 51 (2005) 361–369 369

whales stranded in the southern North Sea during the 1994/1995

winter. Marine Pollution Bulletin 38, 304–313.

IUCN, 1996. IUCN red list of threatened animals. International

Union of Nature and Natural Resources. World Conservation

Union, Gland, Switzerland.

Jarman, W.M., Norstrom, R.J., Muir, D.C.G., Rosenberg, B., Simon,

M., Baird, R.W., 1996. Levels of organochlorine compounds,

including PCDDs and PCDFs, in the blubber of cetaceans from the

west coast of North America. Marine Pollution Bulletin 32, 426–

436.

Johnston, P.A., Stringer, R.L., Santillo, D., 1996. Cetaceans and

environmental pollution: the global concerns. In: Simmonds, M.P.,

Hutchinson, J.D. (Eds.), The Conservation of Whales and

Dolphins. John Wiley and Sons Ltd., Chichester, pp. 219–

261.

Kannan, K., Tanabe, S., Borrell, A., Aguilar, A., Focardi, S.,

Tatsukawa, R., 1993. Isomer-specific analysis and toxic evaluation

of polychlorinated biphenyls in striped dolphins affected by an

epizootic in the western Mediterranean Sea. Archives of Environ-

mental Contamination and Toxicology 25, 227–233.

Kuiken, T., Bennett, P.M., Allchin, C.R., Kirkwood, J.K., Baker, J.R.,

Lockyer, C.H., Walton, M.J., Sheldrick, M.C., 1994. PCBs, cause

of death and body condition in harbour porpoises (Phocoena

phocoena) from British waters. Aquatic Toxicology 28, 13–28.

Langston, W.J., 1990. Toxic effects of metals and the incidence of

metals pollution in marine ecosystems. In: Furness, R.W., Rain-

bow, P.S. (Eds.), Heavy Metals in the Marine Environment. CRC

Press, Boca Raton, FL, pp. 101–122.

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

Blainville�s Beaked Whale (mesoplodon densirostris) stranded in the

United Kingdom. Marine Pollution Bulletin 34, 208–212.

Lund, B., 1994. In vitro adrenal bioactivation and effects on steroid

metabolism of DDT, PCBs and their metabolites in the Grey seal

(Halichoerus grypus). Environmental Toxicology and Chemistry

13, 911–917.

Marsh, H., 1989. Mass stranding of dugongs by a tropical cyclone in

northern Australia. Marine Mammal Science 5, 78–84.

Marsh, H., Breen, B.B., Preen, T., 1994. The status of dugongs, sea

turtles and dolphins in the inshore region of the Great Barrier Reef

Marine Park south of Cape Bedford. James Cook University,

Townsville.

Marsh, H., Corkeron, P., Lawler, I.R., Lanyon, J.M., Preen, A.R.,

1995. The status of the dugong in the southern Great Barrier Reef

Marine Park. James Cook University, Townsville.

Marsh, H., Eros, C., Corkeron, P., Breen, B., 1999. A conservation

strategy for dugongs: implications of Australian research. Marine

and Freshwater Research 50, 979–990.

Marsh, H., Eros, C., Penrose, H., Hugues, J., 2001. The dugong

(Dugong dugon). Status Reports and Action Plans for Countries

and Territories in its range. UNEP.

Miyazaki, N., Itano, K., Fukushima, M., Kawai, S.I., Honda, K.,

1979. Metals and organochlorine compounds in the muscle of

dugong from Sulawesi Island. The Scientific Reports of the Whales

Research Institute 31, 125–128.

Moss, A., Costanzo, S., 1998. Levels of heavy metals in the sediments

of Queensland rivers, estuaries and coastal waters. Royal Austra-

lian Chemical Institute.

Muir, D.C.G., Ford, C.A., Rosenberg, B., Norstrom, R.J., Simon, M.,

Beland, P., 1996. Persistent organochlorines in beluga whales

(Deophinapterus leucas) from the St. Lawrence River estuary—I.

Concentrations and patterns of specific PCBs, chlorinated pesti-

cides and polychlorinated dibenzo-p-dioxins and dibenzofurans.

Environmental Pollution 93, 219–234.

Muller, J.F., Duquesne, S., Ng, J., Shaw, G., Krrishnamohan, K.,

Manonmanii, K., Hodge, M., Eaglesham, G.K., 2000. Pesticides in

sediments from Queensland irrigation channels and drains. Marine

Pollution Bulletin 41, 294–301.

Muller, J.F., Haynes, D., McLachlan, M., Bohme, F., Will, S., Shaw,

G.R., Mortimer, M., Sadlet, R., Connell, D.W., 1999. PCDDs,

PCDFs, PCBs and HCB in marine and estuarine sediments from

Queensland, Australia. Chemosphere 39, 1707–1721.

O�Shea, T.J., 1999. Environmental contaminants and marine mam-

mals. In: Reynolds, J.E., Rommel, S.A. (Eds.), Biology of marine

mammals. Melbourne University Press, Melbourne, pp. 485–536.

O�Shea, T.J., Brownell Jr., R.L., 1994. Organochlorine and metal

contaminants in baleen whales: a review and evaluation of

conservation implications. The Science of the Total Environment

154, 179–200.

O�Shea, T.J., Moore, J.F., Kochman, H.I., 1984. Contaminant

concentrations in manatees in Florida. Journal of Wildlife Man-

agement 48, 741–748.

O�Shea, T.J., Reeves, R.R., Long, A.K. 1999. Marine mammals and

persistent ocean contaminants. Marine Mammal Commission,

Bethesda, Maryland, USA.

Oehme, M., Schlabach, M., Kallenborn, R., Haugen, J.E., 1996.

Sources and pathways of persistent polychlorinated pollutants to

remote areas of the north atlantic and levels in the marine food

chain: a research update. The Science of the Total Environment

186, 13–24.

Parry, D.L., Munksgaard, N.C., 1992. Heavy metal baseline data for

sediment, seawater, and biota, Bing Bong, Gulf of Carpentaria.

Northern Territory University, Darwin.

Parry, D.L., Munksgaard, N.C., 1993. Heavy metal baseline data for

sediment, seawater, and biota, Bing Bong, Gulf of Carpentaria.

Northern Territory University, Darwin.

Preen, A., 1993. Interactions between dugongs and seagrasses in a

subtropical environment. Ph.D. thesis, James Cook University,

Townsville.

Preen, A., 1995. Diet of dugongs: are they omnivores? Journal of

Mammalogy 76, 163–171.

Reijnders, P., 1986. Reproductive failure in common seals feeding on

fish from polluted coastal waters. Nature 324, 456–457.

Spain, A.V., Heinsohn, G.E., 1973. Cyclone associated feeding

changes in the dugong (mammalia: Sirenia). Mammalia 37, 675–

681.

Subramanian, A., Tanabe, S., Tatskawa, R., Saito, S., Miyazaki, N.,

1987. Reduction in testosterone levels by PCBs and DDE in Dall�sporpoises of the North Western North Pacific. Marine Pollution

Bulletin 18, 643–646.

Tanabe, S., Iwata, H., Tatsukawa, R., 1994. Global contamination by

persistent organochlorines and their ecotoxicological impact on

marine mammals. The Science of the Total Environment 154, 163–

177.

Vetter, W., Scholz, E., Gaus, C., Muller, J., Haynes, D., 2001.

Anthropogenic and natural organohalogen compounds in blubber

of dolphins and dugongs (Dugong dugon) from northeastern

Australia. Environmental Contamination and Toxicology 41,

221–231.

Wania, F., Axelman, J., Broman, D., 1998. A review of processes

involved in the exchange of persistent organic pollutants across the

air–sea interface. Environmental Pollution 102, 3–23.

Wilkinson, L., 1996. Systat 7.0 for Windows: Statistics. Microsoft,

Chicago.