Herbicides: A new threat to the Great Barrier Reef

Article (PDF Available)inEnvironmental Pollution 157(8-9):2470-84 · May 2009with80 Reads
DOI: 10.1016/j.envpol.2009.03.006 · Source: PubMed
Abstract
The runoff of pesticides (insecticides, herbicides and fungicides) from agricultural lands is a key concern for the health of the iconic Great Barrier Reef, Australia. Relatively low levels of herbicide residues can reduce the productivity of marine plants and corals. However, the risk of these residues to Great Barrier Reef ecosystems has been poorly quantified due to a lack of large-scale datasets. Here we present results of a study tracing pesticide residues from rivers and creeks in three catchment regions to the adjacent marine environment. Several pesticides (mainly herbicides) were detected in both freshwater and coastal marine waters and were attributed to specific land uses in the catchment. Elevated herbicide concentrations were particularly associated with sugar cane cultivation in the adjacent catchment. We demonstrate that herbicides reach the Great Barrier Reef lagoon and may disturb sensitive marine ecosystems already affected by other pressures such as climate change.
Herbicides: A new threat to the Great Barrier Reef
Stephen E. Lewis
a
,
*
, Jon E. Brodie
a
, Zoe
¨
T. Bainbridge
a
, Ken W. Rohde
b
, Aaron M. Davis
a
,
Bronwyn L. Masters
b
, Mirjam Maughan
a
, Michelle J. Devlin
a
,
Jochen F. Mueller
c
, Britta Schaffelke
d
a
Australian Centre for Tropical Freshwater Research, James Cook University, Townsville, Queensland 4811, Australia
b
Department of Natural Resources and Water, Mackay, Queensland 4740, Australia
c
The University of Queensland, National Research Centre for Environmental Toxicology, Brisbane 4108, Australia
d
Australian Institute of Marine Science, PMB 3, Townsville, Queensland 4810, Australia
Herbicide residues have been detected in Great Barrier Reef catchment waterways and river water plumes which may affect marine ecosystems.
article info
Article history:
Received 21 November 2008
Received in revised form
23 February 2009
Accepted 7 March 2009
Keywords:
Great Barrier Reef
Herbicides
Diuron
Atrazine
Pesticides
abstract
The runoff of pesticides (insecticides, herbicides and fungicides) from agricultural lands is a key concern
for the health of the iconic Great Barrier Reef, Australia. Relatively low levels of herbicide residues can
reduce the productivity of marine plants and corals. However, the risk of these residues to Great Barrier
Reef ecosystems has been poorly quantified due to a lack of large-scale datasets. Here we present results
of a study tracing pesticide residues from rivers and creeks in three catchment regions to the adjacent
marine environment. Several pesticides (mainly herbicides) were detected in both freshwater and coastal
marine waters and were attributed to specific land uses in the catchment. Elevated herbicide concen-
trations were particularly associated with sugar cane cultivation in the adjacent catchment. We
demonstrate that herbicides reach the Great Barrier Reef lagoon and may disturb sensitive marine
ecosystems already affected by other pressures such as climate change.
Crown Copyright Ó 2009 Published by Elsevier Ltd. All rights reserved.
1. Introduction
The health and productivity of coral reefs around the world are in
decline due to climate-change related coral bleaching, over-
harvesting of marine species, outbreaks of the crown-of-thorns
seastar and terrestrial pollution (Brodie et al., 2005; Fabricius, 2005;
Hoegh-Guldberg, 1999; Hughes et al., 2003; Jackson et al., 2001;
Pandolfi et al., 2003; Wilkinson, 2004). Of the world’s coral reef
ecosystems, the Great Barrier Reef (GBR) is among the healthiest
and best managed (Pandolfi et al., 2003; Wilkinson, 2004), although
some coastal and inshore parts of the GBR are considered degraded
by agricultural runoff (Bellwood et al., 2004; Brodie et al., 2007;
DeVantier et al., 2006; Fabricius and De’ath, 2004; Fabricius et al.,
20 05; van Woesik et al., 1999). Hence, the management of agricul-
tural runoff is a key goal in improving the waterquality in the coastal
GBR lagoon (Anon, 2003) and to foster the resilience of marine
ecosystems in the face of climate change (Bellwood et al., 2004;
Hughes et al., 2003; Orr et al., 2005). While there is a relatively good
understanding of the distribution and impacts of land-derived
suspended sediments and nutrients in the GBR (Brodie and Mitchell,
2005; Devlin and Brodie, 20 05; Lewis et al., 2007a; McCulloch et al.,
2003), little is known about pesticide residues.
Herbicide residues have been detected in waterways of the GBR
catchment area (Davis et al., in press; Ham, 2007; McMahon et al.,
2005; Mitchell et al., 2005; Stork et al., 2008) as well as in inter-
tidal/subtidal sediments (Duke et al., 2005; Haynes et al., 2000a),
mangroves (Duke et al., 2005), seagrass (Haynes et al., 2000a) and
waters surrounding inshore coral reefs (Shaw and Mu
¨
ller, 2005),
but pesticide runoff has not previously been traced from the
catchment to the GBR lagoon. River water plumes form in the GBR
lagoon following wet season rains (December to April) that lead to
large water volumes being discharged from the GBR catchment
rivers. These event flows supply virtually all land-based materials
(suspended sediment, nutrients and pesticides) transported
annually to the GBR lagoon (Devlin and Brodie, 2005).
Beef cattle grazing and sugar cane cultivation have been the
dominant industries in the GBR catchment area since the late 19th
century (Fig. 1). The sugar cane industry has undergone major
practice changes over the last three decades including the intro-
duction of minimal tillage practices (Hargreaves et al., 1999; John-
son and Ebert, 2000). These changes, accompanied with the
widespread expansion of the industry on the GBR catchment area
have resulted in a 3–7 fold increase in herbicide use (e.g. atrazine,
*
Corresponding author. Tel.: þ61 7 4781 6629; fax: þ61 7 4781 5589.
E-mail address: stephen.lewis@jcu.edu.au (S.E. Lewis).
Contents lists available at ScienceDirect
Environmental Pollution
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0269-7491/$ see front matter Crown Copyright Ó 2009 Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.envpol.2009.03.006
Environmental Pollution 157 (2009) 2470–2484
diuron and 2,4-D) over the last 30–40 years (Johnson and Ebert,
20 00). Organochlorine insecticides (DDT, aldrin, heptachlor,
chlordane, lindane and dieldrin) were used in the sugar and
horticultural industries from the 1950s and were banned in the
1980s–1990s (Cavanagh et al., 1999). While residues of these
insecticides still persist in sediments and biota of the GBR, they are
thought to pose low risk to marine ecosystems (Cavanagh et al.,
1999; Haynes and Johnson, 2000; Mu
¨
ller et al., 2000; Willis and
McDowell, 1982).
Here we present a comprehensive dataset that examines the
sources, transport and distribution of pesticide residues from
a selection of GBR catchments to the GBR lagoon, including
showing that elevated concentrations of herbicide residues persist
in the GBR lagoon for several weeks after river floods. We then
discuss the potential ecotoxicological risks of these chemicals to the
health and productivity of the GBR.
2. Materials and methods
2.1. Site selection and sample collection in rivers and creeks
From 2005 to 2008, 600 water samples were collected for analyses of pesticide
concentrations from 76 river and creek sites during flood events in three
geographical regions of the GBR catchment area, the Tully–Murray, Burdekin–
Townsville and Mackay Whitsunday regions (Fig. 1; Table 1). These regions collec-
tively represent w35% of the GBR catchment area.
Sampling sites were selected based on land use in the upstream catchment area,
wet season access to the site and the size of the waterway. Sites were established to
target key land uses, including sugar cane cultivation, cattle grazing, urban areas and
undeveloped lands (Supplementary Table 1). The catchment-scale pesticide data are
presented as five specific categories according to area of selected land uses within
the upstream catchment area. These include areas with >10% sugar cane, areas with
0–10% sugar cane, grazing lands with no sugar cane, urban lands with no sugar cane
or grazing, and undeveloped lands. Catchments draining sugar cane also typically
have upper catchment areas of grazing while catchments draining both sugar and
grazing lands may also contain some horticulture. The larger rivers and creeks in the
regions were also studied to examine loads of pesticides exported to the GBR.
Surface water samples (top 50 cm of water column) were collected following
significant rainfall events which triggered stream flow. 1 L samples were collected
from the centre of the channel flow where possible and if samples were collected
from the edge every effort was made to ensure they were collected from the main
flow, away from the backwash at the riverbank. Where possible, a stratified
sampling approach was applied to collect samples over the rising, peak and falling
stages of the flow hydrograph. Water samples were collected in 1 L amber glass
bottles using a sampling pole. The amber bottles were pre-cleaned with acetone and
ethanol and blow-dried with nitrogen gas fitted with a carbon filter. Where it was
not possible to collect samples using the pole, samples were collected in a container
which was rinsed several times with water from the site prior to sample collection.
The water samples were then transported on ice to the Queensland Health Forensic
and Scientific Services (QHFSS) laboratory (Brisbane, Australia) for analysis.
2.2. Flow and load calculations
Gauging stations exist on some of the larger rivers and creeks across the three
regions which allow the calculation of the total volume of water discharged by the
stream. Where representative water samples were collected to encompass the
rising, peak and falling stages of the flow hydrograph, the mass or load of pesticides
exported through the sampled point of the waterway can be calculated. The highest
concentrations of pesticide residues typically occur during the rising limb of the flow
hydrograph before concentrations become diluted with increasing flow (Davis et al.,
in press; Mitchell et al., 2005). Therefore it is critical to sample all stages of the flow
to obtain reliable load estimates. The continuous time series flow data from the
stream-flow gauging stations and point source water quality data were entered into
BROLGA,(version 2.11) a software program which calculates loads using linear
interpolation (Queensland Department of Natural Resources and Water, 2007). This
technique is considered the most suitable to estimate catchment loads with the
available input data (Fox et al., 2005; Letcher et al., 1999; Lewis et al., 2007b).
2.3. Marine sample collection
Surface water samples (top 50 cm of water column) were collected along
transects away from the mouth of the major rivers and creeks in the three
geographical regions. Samples were collected with a container from within and
outside the visible, turbid, plume area from a research vessel, keeping the container
well away from the sides of the boat. While there are possible cross-contamination
issues by using the same sampling container, we believe that it is unlikely that these
relatively polar herbicides (highly soluble in water) be absorbed onto the container.
Salinity was measured in the field using a hand-held refractometer, YSI probe and/or
in the Australian Centre for Tropical Freshwater Research laboratory, James Cook
University (Townsville, Australia) with an electrical conductivity (EC) meter using
reference potassium chloride standards. From 2005 to 2008, 102 surface water
samples were collected for pesticide analyses in the coastal GBR lagoon after
significant river flood events (Fig. 1).
2.4. Analytical methods
The water samples were analysed by liquid chromatography mass spectrometry
(LCMS) and gas chromatography mass spectrometry (GCMS) at the National Asso-
ciation of Testing Authorities accredited QHFSS Laboratory. Organochlorine, organ-
ophosphorus and synthetic pyrethroid pesticides, urea and triazine herbicides and
polychlorinated biphenyls were extracted with dichloromethane and quantified by
GCMS and LCMS (US EPA method 8141, Gan and Bondarenko, 2008, adapted to
analysis of seawater samples by omitting addition of sodium chloride to extrac-
tions). Phenoxyacid herbicides (in selected Burdekin–Townsville catchment samples
only) were extracted with diethyl-ether after acidification, methylated and analysed
by GCMS. Further analytical details are provided in the electronic supplement. Mean
recoveries for diuron and atrazine were 97.5% and 93.0%, respectively with 75% of
the analytes having mean recoveries above 90%. Uncertainties for the pesticide
analytes were typically within 15%.
3. Results
3.1. Pesticides in waterways discharging to the GBR
We detected residues of several pesticides in GBR rivers and
creeks during flood events, including the herbicides diuron, atra-
zine (and associated degradation products desethyl and desiso-
propyl atrazine), hexazinone, ametryn, tebuthiuron, simazine,
metolachlor, bromacil, 2,4-D and MCPA and the insecticides imi-
dacloprid, endosulfan and malathion. The herbicides diuron, atra-
zine (and degradation products), hexazinone and ametryn were
detected frequently and in relatively high concentrations, while
other pesticides were detected only infrequently. Diuron, atrazine,
hexazinone and ametryn were frequently detected at the highest
concentrations at sites draining sugar cane, and the former three
compounds also at sites in the urban land use category (Fig. 2 a–d).
In particular, diuron residues were found at most urban sampling
sites. Diuron is used to control annual and perennial broadleaf and
grassy weeds, not only in sugar cane and croplands but also on
roads, garden paths and railway tracks (Giacomazzi and Cochet,
20 04; Jones et al., 2003). Tebuthiuron residues were only detected
at sites downstream of grazing lands, including some sites which
also drain sugar cane in the lower reaches of the catchment and
were thus classed as ‘sugar’ in our classification scheme (Fig. 2e).
This herbicide is used to control woody plants (McMahon et al.,
20 05) in the beef grazing industry.
Ametryn residues were only detected in waterways draining
sugar cane land use areas and commonly detected in the Burde-
kin–Townsville and Mackay Whitsunday regions. With the
exception of one sample, ametryn residues were only detected at
sites draining >10% sugar cane (Fig. 2d). Simazine residues were
detected at sites draining both sugar cane and urban lands
(Fig. 2f). Simazine is a common product available for use in urban
gardens, although its detection in waterways draining sugar cane
is perplexing as it is not directly used in this industry; the source
of this herbicide may be related to legume fallow crops, weed
control of irrigation drains or product impurities (see Davis et al.,
in press). Simazine residues have been linked to the pine planta-
tion forestry industry (McMahon et al., 2005). However, with the
exception of one site in the Tully–Murray region (out of a total of
17 sites where simazine was detected), residues have been
detected at sites which do not have plantation forestry in the
upstream catchment area.
S.E. Lewis et al. / Environmental Pollution 157 (2009) 2470–2484 2471
S.E. Lewis et al. / Environmental Pollution 157 (2009) 2470–24842472
Of the other pesticides detected during the monitoring program,
metolachlor, bromacil, 2,4-D, MCPA and imidacloprid are products
registered to the sugar cane industry and all detections were
associated with this land use with the exception of bromacil which
was occasionally detected at urban land use sites. Malathion was
detected at only one site draining urban lands and endosulfan was
found at only two sites draining horticulture.
The herbicides 2,4-D and MCPA, and the insecticide imidaclo-
prid were only analysed in the Burdekin–Townsville region
samples and only over one wet season due to analytical costs. Of
these pesticides, 2,4-D and imidacloprid were detected in eight of
17 samples and in four of 18 samples, respectively in the sites
draining sugar cane. 2,4-D residues have previously been detected
in waterways of the Mackay Whitsunday region (Mitchell et al.,
20 05). Metolachlor residues were detected in streams draining
sugar cane and horticulture in only the Burdekin–Townsville
region.
The highest diuron concentrations were 19
m
gL
1
in the Tully–
Murray region, 3.8
m
gL
1
in the Burdekin–Townsville region and
22
m
gL
1
in the Mackay Whitsunday region; all associated with
>10% sugar cane cultivation as the main land use (Fig. 2a). Diuron
residues at the sites draining sugar cane (particularly >10% sugar
cane) were consistently above the ANZECC and ARMCANZ (2000)
ecological trigger value (0.2
m
gL
1
) across all three monitored
regions (Fig. 2a). While the ANZECC and ARMCANZ (2000)
ecological protection trigger values were developed for low flow
conditions, they are the only available reference to assess the risk of
pesticide residues in freshwater environments.
Peak concentrations of atrazine residues were 1.0
m
gL
1
in the
Tully–Murray region, 6.5
m
gL
1
in the Burdekin–Townsville region
and 7.6
m
gL
1
in the Mackay Whitsunday region; all peak
concentrations in these regions were associated with sites draining
>10% sugar cane (Fig. 2b). While atrazine residues were detected at
sites draining grain crops/horticulture and urban lands, the
ANZECC and ARMCANZ (200 0) ecological protection trigger value
was only exceeded at the sites draining sugar cane. In fact, the mean
atrazine concentrations of the >10% sugar cane land use category in
the Burdekin–Townsville and Mackay Whitsunday regions also
exceeded the 99% ANZECC and ARMCANZ (2000) trigger value for
ecological protection (0.7
m
gL
1
), although the median concen-
trations shown in Fig. 2b did not exceed this trigger value. In
addition, the ANZECC and ARMCANZ (2000) 95% trigger value
(13
m
gL
1
) was not exceeded in any sample collected. Both atrazine
and diuron exceeded other internationally recognised water quality
criteria for the protection of aquatic life including the Canadian
Water Quality Guidelines (atrazine: 1.8
m
gL
1
; Nagpal et al., 2006)
and the maximum allowable concentrations specified in the
European Guidelines (diuron: 1.8
m
gL
1
; atrazine 2.0
m
gL
1
; CEC,
20 08). The runoff of diuron and atrazine residues is of particular
concern as these herbicides consistently exceeded trigger values at
sites draining sugar cane areas (Fig. 2a and b).
Tebuthiuron residues reached or exceeded the ANZECC and
ARMCANZ (2000) 99% trigger value for ecological protection
(0.02
m
gL
1
) at five sites in the Burdekin–Townsville region and at
five sites in the Mackay Whitsunday region (Fig. 2e). The ANZECC
and ARMCANZ (2000) national ecological trigger value for
metolachlor (0.02
m
gL
1
) was exceeded in a total of 17 samples
collected from five sites in the Burdekin–Townsville region.
Endosulfan and malathion were only detected in individual
samples in small waterways of the Burdekin–Townsville region
and the risk of these insecticides would be limited to localised
receiving water bodies.
3.2. Pesticide residues in river water plumes
Herbicide residues (diuron, atrazine and hexazinone) were regu-
larly detected in river water plumes in the coastal GBR lagoon adja-
cent to the three monitored catchment regions, particularly in the
plumes adjacent to sugar cane and horticulture lands (Figs. 1, 3–5).
These plumes and associated residues reached mangroves, seagrass
beds and inshore coral reefs. Ametryn and simazine residues were
detected infrequently and only adjacent to the Mackay Whitsunday
region while tebuthiuron residues were only detected in river water
plumes from the Burdekin River (Burdekin–Townsville region) and
the O’Connell River (Mackay Whitsunday region) (Fig. 5).
The herbicide residues displayed conservative mixing behaviour
along the salinity gradient within river water plumes, becoming
increasingly diluted as the river waters progressively mixed with
seawater. The mixing plots (Fig. 6) show that physical, chemical and
biological processes did not remove herbicides, thus herbicides
were detectable to at least 50 km offshore from some river mouths
(Fig. 1) and therefore reach inshore reefs of the GBR lagoon.
Within some plumes, the highest concentrations of herbicide
residues occurred in a zone near the seaward edge of the plume
compared to the samples closer to the river mouth. This most likely
reflects ‘first flush’ waters with typically higher concentrations of
herbicide residues, which were already transported offshore at the
time of sampling (Fig. 6). Diuron, atrazine and tebuthiuron residues in
samples collected offshore from the Mackay Whitsunday region
exceeded locally-derived marine trigger values developed for the
GBR Marine Park (GBRMPA, 2008), and tebuthiuron exceeded the
trigger value in one sample collected in the plume from the Burdekin
River (Figs. 1, 3 and 5).
The river water plumes in the Tully–Murray and Burdekin–
Townsville regions were sampled over 1–2 days, commonly after
peak river discharge had occurred, and only provide a ‘snapshot’ of
herbicide residues in the marine environment. In February 2007,
the river water plumes from the Pioneer (6th and 15th February)
and O’Connell (7th and 16th February) Rivers (Mackay Whitsunday
region) were sampled 9 days apart along the same transect to
investigate the persistence of herbicides over this period. Residues
of diuron, atrazine and hexazinone were detected in the river water
plumes over the two sampling campaigns, whereas simazine and
tebuthiuron residues were below limits of detection in the second
sampling period (Supplementary Table 2). Diuron, atrazine and
hexazinone residues were approximately half the concentrations in
the second sampling period, 9 days later. Time-integrated passive
samplers show that herbicide residues in the GBR lagoon persist
at low concentrations (1–10 ng L
1
range) throughout the year
(Shaw and Mu
¨
ller, 2005), around two orders of magnitude lower
than observed in the river water plumes.
Fig. 1. Great Barrier Reef catchment area, sampling sites, and plume diuron concentration contours. Map of the Great Barrier Reef catchment area (a and b). The three geographic
regions are outlined in red (b). The catchment sampling sites for the Tully–Murray (c), Burdekin–Townsville (d) and Mackay Whitsunday (e) are shown (refer to Table S1 for
summary of catchment sampling sites). The map shows that diuron residues detected in the river water plumes are clearly associated with areas of sugar cane in the adjacent
catchment area. Diuron residues have been commonly detected in river water plumes across the three regions. The contour maps of diuron concentrations in the river water plume
samples across the three regions show that herbicide residues can travel large distances in the marine environment at biologically significant levels. The contour map intervals are
based on the analytical level of detection (0.01
m
gL
1
), the lowest observable effects concentration on marine plants (0.1
m
gL
1
)(Haynes et al., 2000b) and the current GBR water
quality trigger value (0.9
m
gL
1
)(GBRMPA, 2008). The contours are also based on the maximum concentration measured furthest offshore irrespective of year. Refer to Table S3 for
the summary data of the marine samples.
S.E. Lewis et al. / Environmental Pollution 157 (2009) 2470–2484 2473
Table 1
Summary data for the pesticide residues detected at the catchment sampling sites across the three geographical regions.
Site No. Waterway Pesticides detected
None
detected
Atrazine Diuron Hexazinone Ametryn Desethyl
atrazine
Desisopropyl
atrazine
Simazine Malathion Endosulfan Metolachlor MCPA Imidacloprid Bromacil 2,4-D Tebuthiuron
Tully–Murray
1 Nth Hull R. Not
analysed
Not
analysed
Not
analysed2 Porter’s Ck.
3 Banyan Ck. 
4 Bulgan Ck.
5 Banyan Ck. 
6 Jarra Ck.
7 Tully Gorge
8 Davidson Ck. 
9 Davidson Ck.
10 Warrami Ck. 
11 Campbell’s Ck.
12 Kyambul lagoon 
13 Kyambul lagoon 
14 Murray R.
15 Murray R.
16 Murray R. 
17 Tully R. 
18 Marquette Ck.
Burdekin–Townsville
19 Bluewater Ck. Not
analysed
Not
analysed
Not
analysed20 Black R.
21 Bohle R.
22 Kern Drain 
23 Louisa Ck. 
24 Captains Ck.
25 Woolcock St Drain 
26 Gordon Ck. 
27 Alligator Ck.
28 Alligator Ck.
29 Sachs Ck.
30 Ross R.
31 Ross R.
32 Ross Ck. 
33 Campus Ck.
34 Stuart Ck.
35 Stuart Ck.
36 Hen Camp Ck.
37 Don R. 
38 Euri Ck.
39
Yellow
Gin Ck.
40 Iyah Ck. 
41 West Barratta Ck. 
42 East Barratta Ck. 
43 Barratta Ck. 
44 Haughton R. 
45 Sheep Station Ck. 
46 Plantation Ck. 
S.E. Lewis et al. / Environmental Pollution 157 (2009) 2470–24842474
47 Bowen R. Not
analysed
Not
analysed
Not
analysed
48 Suttor R.
49 Belyando R.
50 Cape R.
51 Burdekin R.
Mackay Whitsunday
52 Impulse Ck. Not
analysed
Not
analysed
Not
analysed53 St. Helens Ck.
54 Myrtle Ck. 
55 Andromache R. 
56 Proserpine Drain 
57 Waite Ck.
58 Andromache R.
59 Gregory R. 
60 O’Connell R. 
61 O’Connell R. 
62 O’Connell R. 
63 Proserpine R. 
64 Finch Hatton Ck.
65 Blacks Ck. 
66 Macalister St Drain 
67 Campbell St Drain 
68 McCready’s Ck.
69 Pioneer R. 
70 Sarina Drain 
71 Sandy Ck. 
72 Rocky Dam Ck. 
73 Rocky Dam Ck. 
74 Basin Ck. 
75 Carmila Ck. 
76 Plane Ck. 
S.E. Lewis et al. / Environmental Pollution 157 (2009) 2470–2484 2475
Fig. 2. A summary of herbicide concentrations in waterways draining different land uses. The concentrations of diuron (a), atrazine (b), hexazinone (c) and ametryn (d) residues in
rivers and creeks in the Tully–Murray, Burdekin–Townsville and Mackay Whitsunday regions show a strong land use signal with the highest values associated with increasing area
of sugar cane cultivation in the upstream catchment. However, unlike the other residues associated with sugar, ametryn residues were not detected in the ‘urban’ or ‘grazing’ land
use groupings. In comparison to diuron, atrazine, hexazinone and ametryn residues, tebuthiuron (e) residues from the catchment land use sampling did not show a signal related to
the sugar land use but were associated with grazing lands. The runoff of simazine (f) residues was associated with the sugar and urban land use groupings. Simazine is used in urban
gardens, although its association with sugar is unresolved. The box represents the inter-quartile range containing 50% of the data, with the median shown as the centre line. The
whiskers extend from the box to the highest and lowest concentrations, excluding outliers (circles) which are defined to be outside 1.5 box-lengths (outside the 25th and 75th
percentiles) and extreme values (stars) which are defined to be outside 3 box-lengths. The ANZECC and ARMCANZ (2000) national freshwater ecological trigger values for diuron
and atrazine are included for comparison (dashed lines).
S.E. Lewis et al. / Environmental Pollution 157 (2009) 2470–24842476
4. Discussion
The pesticide residues detected in the waterways of the GBR
catchment area are of concern to coastal water bodies. While the
runoff of diuron, atrazine, hexazinone and ametryn residues from
GBR catchment waterways draining sugar cane lands has previously
been reported (Davis et al., in press; Ham, 2007; McMahon et al.,
2005; Mitchell et al., 2005; Stork et al., 2008), our data show that
runoff of these residues from regions dominated by sugar cane is
widespread. In the larger streams of the Burdekin–Townsville and
Mackay Whitsunday regions, the combined loads of diuron, atrazine
and hexazinone (active ingredients only) were in the order of
hundreds of kilograms per large flow event (Table 2). A typical flow
event in these waterways would last for approximately 3–5 days
Fig. 2. (continued).
S.E. Lewis et al. / Environmental Pollution 157 (2009) 2470–2484 2477
Fig. 3. Great Barrier Reef catchment area, sampling sites, and plume atrazine concentration contours. Atrazine residues have been frequently detected in river water plumes across
the three regions. The contour maps have been constructed based on the analytical level of detection (0.01
m
gL
1
), the locally derived ecological protection trigger value for the GBR
(0.4
m
gL
1
)(GBRMPA, 2008) and the lowest observable effects concentration (3
m
gL
1
)(Jones and Kerswell, 2003). The contours are based on the maximum concentration
measured furthest offshore irrespective of year. While the marine ecological protection trigger value for atrazine was only exceeded near the Pioneer River mouth in the Mackay
Whitsunday region, this herbicide was commonly detected in combination with diuron and hexazinone residues. We note that the lowest observable effects concentration of
atrazine exposure on marine pla nts was not exceeded in any river water plume samples. Refer to Supplementary Table 2 for the summary data of the marine samples.
Fig. 4. Great Barrier Reef catchment area, sampling sites, and plume hexazinone concentration contours. Hexazinone residues were frequently detected in river water plumes
offshore from the Tully–Murray and Mackay Whitsunday regions. The contour maps have been constructed based on the analytical level of detection (0.01
m
gL
1
), the lowest
observable effects concentration (3
m
gL
1
)(Jones and Kerswell, 2003) and the locally-derived marine trigger value (75
m
gL
1
)(GBRMPA, 2008). The contours are based on the
maximum concentration measured furthest offshore irrespective of year. While neither the lowest observable effects concentration nor the marine ecological protection trigger
value was exceeded, hexazinone in combination with diuron and atrazine residues produce an additive mixture of photosystem II inhibitors.
Fig. 5. Great Barrier Reef catchment area, sampling sites, and plumetebuthiuron concentration contours. Tebuthiuron residues were detected offshore from the BurdekinRiver(Burdekin–
Townsville region) and from the O’Connell River (Mackay Whitsunday region). The marine ecological protection trigger value was exceeded offshore from the mouths of these rivers,
although the residues were below lowest observable effects concentration. The contour maps have been constructed based on the analytical level of detection (0.01
m
gL
1
), the locally-
derived marine ecological protection trigger value (0.02
m
gL
1
)(GBRMPA, 2008) and the lowest observable effects concentration (10
m
gL
1
)(Jones and Kerswell, 2003). The contours are
based on the maximum concentration measured furthest offshore irrespective of year. Tebuthiuron is used to control woody weeds in the beef grazing industry and its detection in the
larger streams across the Burdekin–Townsville and Mackay Whitsunday regions suggest that large loads of this herbicide may be exported to the GBR during river flow events.
where the majority of these loads would be exported. Because our
monitoring sites did not always represent the entire catchment area,
total ‘end-of-catchment’ loads to the GBR lagoon may be even
higher. The measured export of diuron alone to the GBR lagoon from
the Pioneer River has exceeded 300 kg in each major flow event over
three years of monitoring (Table 2). The event mean concentrations
for the streams where loads could be calculated exceeded ANZECC
and ARMCANZ (2000) trigger values for both diuron and atrazine
(Table 2). In the Burdekin and O’Connell Rivers, tebuthiuron residues
were also detected in large flow events (Table 1).
The mixing profiles of diuron, atrazine, and hexazinone residues
in the river water plumes over the salinity gradient (Fig. 6) show
that physical, chemical and biological processes were not removing
herbicides in flood waters during the mixing/dilution with
seawater. This result also suggests that herbicide residues are in the
dissolved phase rather than bound to particulate materials. The
physical removal of sediments near the mouth of the river via
flocculation processes would show non-linear characteristics as
would the chemical degradation of the herbicide products or
uptake by biota. Nevertheless, even if some herbicide residues are
bound to fine sediment particles, they remain highly bioavailable to
marine organisms (see Harrington et al., 2005).
Biologically significant concentrations (exceedi ng lowest
observable effects concentration: Haynes et al., 2000b) of d iuron
were found in the river water plu mes from the Tully–Murray and
Mackay Whitsunday regions while the locally derived ecological
protection trigger value for the GBR lagoon (GBRMPA, 2008) was
exceeded offshore from the mouth of the Pioneer River (Mackay
Whitsunday region) (Fig. 1). Similarly, the marine ecological
protection trigger value f or atrazine (GBR MPA, 2008)(Fig. 3) was
only exceeded offshore from the Pioneer River, although th e
current lowest observable ef fect concentration (Jones and Ker-
swell, 2003) was not. Hexazinone residues (Fig. 4) were detectable
offshore from the Tully River (Tully–Murray), Ross River
Fig. 6. Diuron, atrazine and hexazinone concentrations over the plume salinity gradient. Herbicide residues typically displayed a downward linear mixing trend along the salinity
gradient becoming increasingly diluted as the river plume water becomes mixed with seawater. A downward linear trend is observed over the salinity gradient (in practical salinity
units: PSU) for diuron (a), atrazine (b) and hexazinone (c) residues in a river water plume measured in the Mackay Whitsunday region in 2007. Anomalously high concentrations can
occur in the mid-salinity zone (w10–15 PSU) where herbicide residues do not co nform to the initial downward linear trend. These concentrations are probably an artefact of the
‘first flush’ behaviour (shown in a and c) where the highest pollutant concentrations are commonly measured in catchment waterways.
S.E. Lewis et al. / Environmental Pollution 157 (2009) 2470–2484 2481
(Burdekin–Townsville), O’Connell River and Pioneer River
(Mackay Whitsund ay) but conc entrations were well below any
known effects level (Jon es and Kerswell, 20 03) or the marine
trigger value (GBRMPA, 2008). Tebuthiuron residues (Fig. 5) were
detected offshore from the Burdekin and O’Connell Rivers and
some of these sa mples exceeded the loc ally derived ecological
protection trigger value for the GBR (GBRMPA, 2008). This trigger
value was exceeded >20 km offshore from the mouths of these
rivers (Fig. 5). Three herbicide products (diuron, atrazine and
tebuthiu ron) measured in the GBR lagoon exceeded known effect
concentrations (H aynes et al., 2000b; Jones and Kerswell, 2003 )
and/or locally derived ecological protection trigger values for the
GBR (GBRMPA, 20 08) offshore from the mout hs of the Tully,
Burdekin, O’Connell and Pioneer Rivers. Whil e these significant
herbicide concentrations (above either effect levels or ecological
protection trigger values) indicate a risk to the immediate inshore
areas of the GBR lagoon, the risk may extend further offshore d ue
to the comb ination of these photosystem II-inhibiting residues in
the river water plumes.
Levels of herbicide residues in river water plumes in the GBR
lagoon can reach levels that present a risk to GBR ecosystems.
Laboratory-based ecotoxicological tests show that marine photo-
synthetic organisms are vulnerable to herbicide exposure,
including macroalgae (Magnusson et al., 2008; Seery et al., 2006),
mangroves (Bell and Duke, 2005), seagrass (Haynes et al., 2000b)
and corals (Cantin et al., 2007; Jones, 2005; Jones and Kerswell,
20 03; Jones et al., 2003; Negri et al., 2005; Owen et al., 2003) with
certain species more sensitive than others. For example, the
mangrove Avicennia marina is more sensitive to diuron and ame-
tryn residues than other mangrove species (Bell and Duke, 2005).
Similarly in seagrass species, the lowest observable effect concen-
trations of diuron exposure can be up to two orders of magnitude
different for the species Halophila ovalis and Zostera capricorni (both
0.1
m
gL
1
) compared to Cymodocea serrulata (10
m
gL
1
)(Haynes
et al., 2000b). Differences in effect concentrations have also been
measured in the early development (Negri et al., 2005) and
reproduction stages (Cantin et al., 2007) of various coral species.
However, these differences have not been observed in zooxan-
thellae (either in symbio or in vitro) from various coral species
(Jones, 2005; Jones and Kerswell, 2003; Owen et al., 2003).
The assessment of risk of herbicide exposure in the GBR is
further complicated by the different toxicity of various herbicides.
Studies on the same species of marine plants have shown that
diuron affects photosynthesis at lower doses than for example,
atrazine, hexazinone or tebuthiuron (Bell and Duke, 2005; Jones,
2005; Jones and Kerswell, 2003; Jones et al., 2003; Magnusson
et al., 2008; Owen et al., 2003; Ralph, 2000; Seery et al., 2006 ). In
addition, the toxicities of degradation products of herbicide resi-
dues in the GBR lagoon are largely unstudied and may be equal or
greater than toxicities of the parent compounds (see Giacomazzi
and Cochet, 2004; Graymore et al., 2001; Stork et al., 2008).
The mode of action of the herbicides detected in the river water
plumes in the GBR lagoon is to inhibit the photosystem II in plants,
a key component of the photosynthetic apparatus (Jones et al.,
2003). A combination of herbicides is likely to have additive effects
(Bengtson Nash et al., 2005, 2006). A method to normalise herbi-
cide products to a standard toxicity index has been developed to
account for the relative toxicities of the various herbicide products
(Bengtson Nash et al., 2005, 2006), although there is a lack of data
for certain herbicides and their comparative toxicity. These
complexities of herbicide mixtures reduce the capacity to quantify
the risk of herbicide exposure in the GBR lagoon.
Other herbicide products, which have been found in the
waterways of the monitored regions and thus have the potential to
travel offshore, have different modes of action compared to the
photosystem II-inhibiting herbicides. The product 2,4-D, for
example, acts as a plant growth regulator (Owen et al., 2003). 2,4-D
has been shown to be toxic to the salt excluding mangrove species
(Walsh et al., 1973) compared to the photosystem II herbicides
which are more toxic to the salt-excreting mangrove species (Bell
and Duke, 2005). 2,4-D residues were not analysed in the river
water plumes in this study, but this herbicide was detected in some
streams in the Burdekin–Townsville region (Table 1; Davis et al., in
press) and in the Mackay Whitsunday region (Mitchell et al., 2005).
The combination of 2,4-D with photosystem II inhibitors may have
the potential to induce synergistic effects on marine plants. In
addition, the detection of other non-photosystem II herbicides in
the catchment samples such as metolachlor (a growth inhibitor of
seedings) as well as the detection of the insecticide imidacloprid
has potential to cause enhanced effects on freshwater and marine
organisms.
Table 2
Loads of herbicides (kg) and event mean concentrations (EMC:
m
gL
1
) exported from waterways.
Site Year Flow
(ML)
Diuron
(kg)
Diuron EMC
(
m
gL
1
)
Atrazine
(kg)
Atrazine EMC
(
m
gL
1
)
Hexazinone
(kg)
Hexazinone EMC
(
m
gL
1
)
West Barratta Creek 2005/06 138,200 46 0.33 80 0.58 2.7 0.02
2006/07 150,500 79 0.52 116 0.77 2.2 0.01
2007/08 176,000 44 0.25 70 0.40 1.0 0.01
Haughton River 2005/06 254,600 63 0.25 72 0.28 þ
2006/07 530,000 39 0.07 26 0.05 BDL
2007/08 256,000 16 0.06 25 0.10 BDL
Pioneer River 2001/02
a
126,000 470 3.73 75 0.60 28 0.22
2004/05 207,000 310 1.50 95 0.46 45 0.22
2006/07 415,000 470 1.13 310 0.75 140 0.34
Sandy Creek 2002/03
a
21,000 26 1.24 BDL BDL
2004/05 67,000 180 2.69 40 0.60 36 0.54
2006/07 130,000 200 1.54 66 0.51 73 0.56
O’Connell River 2004/05 65,000 17 0.26 3.7 0.06 2.5 0.04
2005/06 61,000 30 0.49 6.6 0.11 4.9 0.08
2006/07 27,000 31 1.15 20 0.74 2.5 0.09
EMC: Event mean concentration.
BDL: No load calculated as concentrations were below the analytical limit of detection (0.01
m
gL
1
); þ No load calculated as only a single sample with concentration above
analytical detection.
a
Mitchell et al., 2005.
S.E. Lewis et al. / Environmental Pollution 157 (2009) 2470–24842482
Herbicides may act in synergy with other chemical pollutants and
environmental stressors (e.g. excess suspended sediments or nutri-
ents, increasing temperature, reduced salinity during floods) and
adversely affect corals and marine algae (Harrington et al., 2005;
Jones and Kerswell, 2003). However, preliminary studies reported
that enhanced or additive effects of salinity and temperature in
combination with herbicides are negligible (Jones, 2005; Jones and
Kerswell, 2003). The dearth of studies on synergistic effects also
limits our ability to assess the risk of pesticides to GBR organisms.
The majority of ecotoxicological studies quantified short-term
effects of herbicide exposure (exposure times of hours to days)
using pulse amplitude modulation chlorophyll fluorescence tech-
niques as a measure of effective quantum yield of the photosystem
of the target plant (e.g. Bell and Duke, 2005; Haynes et al., 2000b;
Jones, 2005; Macinnis-Ng and Ralph, 2003; Magnusson et al.,
20 08). Lowest observable effect concentrations (decline in
quantum yield) in these experiments have been recorded within
hours of exposure at levels as low as 0.1
m
gL
1
(Haynes et al.,
20 00b), although most species recovered after the exposure ceased
(Haynes et al., 2000b; Jones, 2005; Jones and Kerswell, 2003; Jones
et al., 2003; Negri et al., 2005). However, chronic effects of longterm
herbicide exposure to GBR plant communities would develop over
a longer timeframe. Our results show that herbicide residues can
persist in the GBR lagoon over longer timescales (weeks) than the
exposure times applied in most ecotoxicological studies. A decline
in the reproductive output of corals was reported following diuron
exposure over a period of 50 days (Cantin et al., 2007). In addition,
chronic exposure to diuron (and possibly ametryn) residues has
been implicated as the cause of severe mangrove dieback of A.
marina in the Mackay Whitsunday region which has developed
progressively over a 10 year period (Duke et al., 2005).
While the risk of herbicide runoff to GBR ecosystems can be
inferred from measured concentrations in river water plumes
coupled with data from laboratory-based ecotoxicological studies,
there are no field data of biological damage to directly link herbi-
cide runoff to degradation of coral reefs. Degradation of coral reef
ecosystems has been reported from sites immediately adjacent to
the Tully–Murray (Fabricius et al., 2005; DeVantier et al., 2006) and
Mackay Whitsunday (van Woesik et al., 1999) regions. This degra-
dation has been linked to poor water quality from agricultural
runoff, although the relative importance of the various components
of land-runoff (herbicides, excess suspended sediments and
nutrients) is unresolved. Ongoing water quality monitoring in
combination with regular status evaluations of coral reef health
will provide data for future correlative assessments (Schaffelke
et al., 20 08).
5. Conclusions
The risk of herbicide residues in the GBR lagoon is difficult to
quantify because of the scarcity of ecotoxicological studies that test
chronic and interactive effects of these man-made pollutants.
Applying the results from short-term exposure experiments indi-
cates that the herbicide levels from flood-affected coastal waters of
the GBR lagoon reported in this study would negatively affect some
marine organisms, at least temporarily. We predict that the mixture
of herbicide residues following river discharge events has the
capacity to produce cumulative chronic effects on sensitive species
of marine plants and corals. These effects may cause a change in the
community structure of mangrove, seagrass and coral reef
ecosystems. Differences in coral reef species assemblages on
inshore coral reefs of the GBR adjacent to agricultural lands
(including offshore from the Tully–Murray and Mackay Whit-
sunday regions) have been linked to effects of land-runoff, chiefly
showing decreased biodiversity and abundance of corals but
increased abundances of macroalgae in areas most exposed to land-
runoff (DeVantier et al., 2006; Fabricius and De’ath, 2004; Fabricius
et al., 2005; van Woesik et al., 1999). However, the relative
importance of the various components of land-runoff (herbicides,
excess suspended sediments and nutrients) is unresolved.
Our data show that most of the herbicide residues detected in
the GBR lagoon (diuron, atrazine, hexazinone and ametryn) can be
attributed to application in sugar cane cultivation. Tebuthiuron, on
the other hand, is clearly linked to beef grazing management
practices. The development of improved management practices in
agricultural lands is required to reduce the risk of exposure to
terrestrial pollutants, such as herbicides, in the receiving marine
environments. At present, the sugar, horticulture and grazing
industries adjacent to the GBR as well as government agencies are
beginning to address this challenge, allowing moderate optimism
for the long-term resilience of the Great Barrier Reef.
Acknowledgements
We thank Tim Cooper, Katharina Fabricius (Australian Institute
of Marine Science), Damon Sydes (Cassowary Coast Regional
Council) and David Green (Queensland Natural Resources and
Water: NRW) for collecting the water samples in the Tully–Murray
Region. Joelle Prange and Paul Groves (Great Barrier Reef Marine
Park Authority) helped to collect river water plume samples
offshore from the Burdekin–Townsville region. Natalie Fries (NRW)
and Sarina, Mackay and Whitsunday catchment group members
helped to collect samples in the Mackay Whitsunday region. Dr
Lionel Glendenning (Australian Centre for Tropical Freshwater
Research) provided a review of an earlier version of this manu-
script. EnTox is co-founded by Queensland Health. This project was
funded by the Australian Government’s Marine and Tropical
Sciences Research Facility, Burdekin Dry Tropics NRM, Mackay
Whitsunday NRM, Terrain NRM and Townsville City Council Creek
to Coral. We thank the Queensland Health Forensic and Scientific
Services (QHFSS) laboratory for analysing the pesticide samples and
particularly Simon Christen (QHFSS) who provided additional
details on the analytical method.
Appendix. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at
doi:10.1016/j.envpol.2009.03.0 06.
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S.E. Lewis et al. / Environmental Pollution 157 (2009) 2470–24842484
    • "We assessed the response of benthic diatoms to eight different herbicides commonly found as contaminants in rivers within the GBR catchment area, North Queensland, Australia (Lewis et al., 2009). The eight herbicides chosen account for a vast majority of the herbicide load in the region, with the PSII inhibitors atrazine and diuron together accounting for approximately 90% of the measured loads within rivers of the GBR catchment area (Davis et al., 2012). "
    [Show abstract] [Hide abstract] ABSTRACT: Herbicides are common pollutants of rivers in agricultural regions. These contaminants include various types of chemicals with different modes of toxic action. Herbicides can have toxic effects on freshwater benthic diatoms, the base of the aquatic food web. We examined the effects of (non-mixture) herbicide exposure to the health of diatoms for eight common herbicides with three different modes of action; the photosystem II (PSII) inhibitors: atrazine, simazine, hexazinone, tebuthiuron and diuron; two auxinic herbicides: MCPA and 2,4-D; and the EPSP synthase inhibitor: glyphosate. Benthic diatoms within riverine communities were exposed to each herbicide in rapid toxicity tests at concentrations of 50, 200 and 500μgL(-1). The most sensitive taxa were Gomphonema spp. and Encyonema gracilis. Navicula cryptotenella was the most tolerant to herbicide exposure. There was no significant effect of the different herbicide modes of action at the community level. Herbicide mode of action did not alter which taxa were most sensitive within the community and sensitivity rankings of the dominant diatom taxa were similar for each of the eight herbicides. The consistency of the results between herbicides suggests that freshwater benthic diatoms may be suitable in situ indicators for detecting the toxicity of herbicides with differing modes of action.
    Full-text · Article · Jul 2016
    • "An additional seawater sample was collected in the tropical dry season (13 October 2009), north of Dunk Island, QLD, Australia (latitude −17.9242918, longitude 146.1429637) (Fig. S1). This site is ∼15 km downstream from the Tully River mouth, and exposed to diuron and other PSII herbicides in comparable concentrations as the Cape Ferguson site (Lewis et al., 2009; Kennedy et al., 2012a; Kennedy et al., 2012b). A 20 L volume was taken from a depth of 5 m and pre-filtered through a 2.7 µm Whatman GF/D filter and a 1.6 µm Whatman GF/A filter to remove particles and most eukaryotic microorganisms. "
    [Show abstract] [Hide abstract] ABSTRACT: Diuron is a herbicide commonly used in agricultural areas where excess application causes it to leach into rivers, reach sensitive marine environments like the Great Barrier Reef (GBR) lagoon and pose risks to marine life. To investigate the impact of diuron on whole prokaryotic communities that underpin the marine food web and are integral to coral reef health, GBR lagoon water was incubated with diuron at environmentally-relevant concentration (8 µg/L), and sequenced at specific time points over the following year. 16S rRNA gene amplicon profiling revealed no significant short- or long-term effect of diuron on microbiome structure. The relative abundance of prokaryotic phototrophs was not significantly altered by diuron, which suggests that they were largely tolerant at this concentration. Assembly of a metagenome derived from waters sampled at a similar location in the GBR lagoon did not reveal the presence of mutations in the cyanobacterial photosystem that could explain diuron tolerance. However, resident phages displayed several variants of this gene and could potentially play a role in tolerance acquisition. Slow biodegradation of diuron was reported in the incubation flasks, but no correlation with the relative abundance of heterotrophs was evident. Analysis of metagenomic reads supports the hypothesis that previously uncharacterized hydrolases carried by low-abundance species may mediate herbicide degradation in the GBR lagoon. Overall, this study offers evidence that pelagic phototrophs of the GBR lagoon may be more tolerant of diuron than other tropical organisms, and that heterotrophs in the microbial seed bank may have the potential to degrade diuron and alleviate local anthropogenic stresses to inshore GBR ecosystems.
    Full-text · Article · Mar 2016
    • "In the Water Framework Directive (2000/60/EC), diuron, and later irgarol (Directive 2013/39/UE), were included in the list of " 48 priority pollutants to be monitored in European waters " , which will lead to their progressive prohibition over the next 20 years. While diuron is no longer used in most European countries, it is still of great concern in other countries, such as in Australia where it is known to be harmful to the Great Barrier Reef (Lewis et al., 2009; Holmes, 2012 ). In contrast, irgarol is still widely used in antifouling paints all around the world despite reports of high toxicity in some studies from the U.K. (Thomas et al., 2001; Chesworth et al., 2004), where its use in antifouling paints has been prohibited. "
    [Show abstract] [Hide abstract] ABSTRACT: A wild strain of Chaetoceros calcitrans and wild and diuron-resistant strains of Tetraselmis suecica, were exposed to the PSII inhibitor herbicides diuron and irgarol, individually and in mixtures. The effects of three concentrations of diuron and irgarol and four binary mixtures were evaluated on doubling time, relative reactive oxygen species and lipid content by flow cytometry, and on photosynthetic efficiency by pulse amplitude modulated fluorescence. In both wild strains, significant effects were observed for each molecule at the highest concentration tested: at irgarol 0.5 μg L(-1), C. calcitrans was shown to be more sensitive than T. suecica (+52% and +19% in doubling time, respectively), whereas at diuron 5 μg L(-1), T. suecica was more affected (+125% in doubling time) than C. calcitrans (+21%). Overall, irgarol had a higher toxicity at a lower concentration than diuron (no effect at diuron 0.5 μg L(-1)) for both wild strains. The strongest mixture (irgarol 0.5 μg L(-1) + diuron 5 μg L(-1)) increased doubling time by 356% for T. suecica, thus showing amplified effects when the two compounds were mixed. Sequencing of the diuron-resistant strain demonstrated a single mutation in the psbA gene coding sequence. Although resistance of this strain to diuron was confirmed with no effect at the highest diuron concentration, no resistance to irgarol was shown. In addition, the mutant strain exposed to the strongest mixture showed a 3.5-fold increase in doubling time compared with irgarol alone, thereby supporting the hypothesis of a biochemical interaction between these two compounds.
    Full-text · Article · Mar 2016
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