Herbicides: a new threat to the Great Barrier Reef.
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.
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ABSTRACT: Field studies of diuron and its metabolites 3-(3,4-dichlorophenyl)-1-methylurea (DCPMU), 3,4-dichlorophenylurea (DCPU) and 3,4-dichloroaniline (DCA) were conducted in a farm soil and in stream sediments in coastal Queensland, Australia. During a 38 week period after a 1.6 kg ha(-1) diuron application, 70-100% of detected compounds were within 0-15 cm of the farm soil, and 3-10% reached the 30-45 cm depth. First-order t(1/2) degradation averaged 49+/-0.9 days for the 0-15, 0-30 and 0-45 cm soil depths. Farm runoff was collected in the first 13-50 min of episodes lasting 55-90 min. Average concentrations of diuron, DCPU and DCPMU in runoff were 93, 30 and 83-825 microg L(-1) respectively. Their total loading in all runoff was >0.6% of applied diuron. Diuron and DCPMU concentrations in stream sediments were between 3-22 and 4-31 microg kg(-1) soil respectively. The DCPMU/diuron sediment ratio was >1. Retention of diuron and its metabolites in farm topsoil indicated their negligible potential for groundwater contamination. Minimal amounts of diuron and DCMPU escaped in farm runoff. This may entail a significant loading into the wider environment at annual amounts of application. The concentrations and ratio of diuron and DCPMU in stream sediments indicated that they had prolonged residence times and potential for accumulation in sediments. The higher ecotoxicity of DCPMU compared with diuron and the combined presence of both compounds in stream sediments suggest that together they would have a greater impact on sensitive aquatic species than as currently apportioned by assessments that are based upon diuron alone.Pest Management Science 06/2008; 64(9):954-63. · 2.59 Impact Factor
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ABSTRACT: Previous studies have provided evidence for greater sediment input into the inner Great Barrier Reef (GBR) since the mid-nineteenth century, presumably caused by an increase in erosion due to intensive animal grazing after European settlement. Here we report a new trace element (Ba, Y, Mn) study of a Porites coral from Magnetic Island, northeastern Australia that grew continuously for 175 yr from 1813–1986. Increasing Ba and Y concentrations in the 1850–1890 coral growth bands are attributed to increased soil erosion caused by the introduction of livestock, mainly cattle, into the adjacent Burdekin River catchment, the largest contributor of suspended sediment to the GBR lagoon. In our study Y levels continued to rise with agricultural intensification; however, Ba concentrations reach a plateau after 1890, indicating that Ba/Ca ratios in near-shore corals may reflect additional factors than sediment input.Mn concentrations in the coral follow a more complicated pattern, which is clearly related to changes in catchment land-use and related erosion. Before the initiation of European settlement and the introduction of sheep into the Burdekin River catchment in 1854, coral Mn concentrations were uniformly low (< 1 ppm), yielding typical values for coral aragonite. However, after 1854, coral Mn levels rose dramatically, fluctuating in parallel with livestock numbers but with ever smaller amplitudes before reaching more normal values again by 1900. The coincidence in timing between the initial rise in coral Mn and the introduction of grazing animals in the Suttor and Belyando sub-catchments pinpoints the trace element source as the Burdekin River. A decrease in Mn levels since 1865 against a background of generally increasing land clearing, livestock numbers and sediment flux points to the existence of a transient, surficial Mn reservoir in the southern Burdekin River catchment, which is tentatively identified here as the pre-European topsoil on the Peak Range basaltic province. A brief return to moderate Mn levels between 1945–1960 is attributed to the expansion of the cattle industry into the upper Burdekin, Bowen and Suttor sub-catchments after World War II.This geochemical record confirms that trace elements in massive corals can be used to trace sediment input from neighbouring river catchments. In our study, Y concentrations are closely correlated with predicted increases in sediment flux due to land-use changes and prolonged droughts and so may be more useful than Ba for this purpose. Our Mn results attest to the rapidity of the ecosystem imbalance caused by the introduction of grazing animals, in particular, sheep into NE Australia. Within 30 yr, sheep had efficiently reworked and entirely removed the Mn-rich topsoil, which had conceivably accumulated during thousands of years of regular burning by Australia's indigenous population.Palaeogeography, Palaeoclimatology, Palaeoecology. 01/2007;
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ABSTRACT: Today's surface ocean is saturated with respect to calcium carbonate, but increasing atmospheric carbon dioxide concentrations are reducing ocean pH and carbonate ion concentrations, and thus the level of calcium carbonate saturation. Experimental evidence suggests that if these trends continue, key marine organisms—such as corals and some plankton—will have difficulty maintaining their external calcium carbonate skeletons. Here we use 13 models of the ocean–carbon cycle to assess calcium carbonate saturation under the IS92a 'business-as-usual' scenario for future emissions of anthropogenic carbon dioxide. In our projections, Southern Ocean surface waters will begin to become undersaturated with respect to aragonite, a metastable form of calcium carbonate, by the year 2050. By 2100, this undersaturation could extend throughout the entire Southern Ocean and into the subarctic Pacific Ocean. When live pteropods were exposed to our predicted level of undersaturation during a two-day shipboard experiment, their aragonite shells showed notable dissolution. Our findings indicate that conditions detrimental to high-latitude ecosystems could develop within decades, not centuries as suggested previously.Nature 09/2005; 437(7059):681-686. · 38.60 Impact Factor
Herbicides: A new threat to the Great Barrier Reef
Stephen E. Lewisa,*, Jon E. Brodiea, Zoe ¨ T. Bainbridgea, Ken W. Rohdeb, Aaron M. Davisa,
Bronwyn L. Mastersb, Mirjam Maughana, Michelle J. Devlina,
Jochen F. Muellerc, Britta Schaffelked
aAustralian Centre for Tropical Freshwater Research, James Cook University, Townsville, Queensland 4811, Australia
bDepartment of Natural Resources and Water, Mackay, Queensland 4740, Australia
cThe University of Queensland, National Research Centre for Environmental Toxicology, Brisbane 4108, Australia
dAustralian 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.
a r t i c l e i n f o
Received 21 November 2008
Received in revised form
23 February 2009
Accepted 7 March 2009
Great Barrier Reef
a b s t r a c t
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 ? 2009 Published by Elsevier Ltd. All rights reserved.
decline due to climate-change related coral bleaching, over-
harvesting of marine species, outbreaks of the crown-of-thorns
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
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.,
2005; van Woesik et al., 1999). Hence, the management of agricul-
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; Orret al., 2005). While there is a relativelygood
understanding of the distribution and impacts of land-derived
2005; Devlin and Brodie, 2005; 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
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: firstname.lastname@example.org (S.E. Lewis).
Contents lists available at ScienceDirect
journal homepage: www.elsevier.com/locate/envpol
0269-7491/$ – see front matter Crown Copyright ? 2009 Published by Elsevier Ltd. All rights reserved.
Environmental Pollution 157 (2009) 2470–2484
diuron and 2,4-D) over the last 30–40 years (Johnson and Ebert,
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
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 keyland 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 mayalso 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
concentrationsof pesticide residuestypicallyoccurduring 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%.
3.1. 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,
2004; 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.,
2005) 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 detectedduring 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.,
2005). Metolachlor residues were detected in streams draining
sugar cane and horticulture in only the Burdekin–Townsville
The highest diuron concentrations were 19 mg L?1in the Tully–
Murray region, 3.8 mg L?1in the Burdekin–Townsville region and
22 mg L?1in 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 mg L?1) across all three monitored
regions (Fig. 2a). While the ANZECC and ARMCANZ (2000)
ecological protection trigger values were developed for low flow
conditions, theyare the only available reference to assess the risk of
pesticide residues in freshwater environments.
Peak concentrations of atrazine residues were 1.0 mg L?1in the
Tully–Murray region, 6.5 mg L?1in the Burdekin–Townsville region
and 7.6 mg L?1in 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 (2000) ecological protection trigger value
was onlyexceeded at the sitesdraining sugarcane. In fact, the mean
atrazine concentrations of the >10% sugarcane 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 mg L?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 mg L?1) was not exceeded in any sample collected. Both atrazine
and diuronexceeded other internationally recognised waterquality
criteria for the protection of aquatic life including the Canadian
Water Quality Guidelines (atrazine: 1.8 mg L?1; Nagpal et al., 2006)
and the maximum allowable concentrations specified in the
European Guidelines (diuron: 1.8 mg L?1; atrazine 2.0 mg L?1; CEC,
2008). 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 mg L?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 mg L?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
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
triggervalueinonesamplecollectedintheplume fromthe 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?1range) 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 mg L?1), the lowest observable effects concentration on marine plants (0.1 mg L?1) (Haynes et al., 2000b) and the current GBR water
quality trigger value (0.9 mg L?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) 2470–24842473
Summary data for the pesticide residues detected at the catchment sampling sites across the three geographical regions.
Site No. Waterway Pesticides detected
Nth Hull R.
21 Bohle R.
22 Kern Drain
25 Woolcock St Drain
26 Gordon Ck.
28 Alligator Ck.
31 Ross R.
34 Stuart Ck.
36Hen Camp Ck.
38 Euri Ck.
Yellow Gin Ck.
41 West Barratta Ck.
42East Barratta Ck.
43 Barratta Ck.
45 Sheep Station Ck.
S.E. Lewis et al. / Environmental Pollution 157 (2009) 2470–2484
53St. Helens Ck.
54 Myrtle Ck.
59 Gregory R.
64Finch Hatton Ck.
66 Macalister St Drain
67Campbell St Drain
69 Pioneer R.
72Rocky Dam Ck.
73Rocky Dam Ck.
75 Carmila Ck.
76 Plane Ck.
S.E. Lewis et al. / Environmental Pollution 157 (2009) 2470–2484
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
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 mg L?1), the locally derived ecological protection trigger value for the GBR
(0.4 mg L?1) (GBRMPA, 2008) and the lowest observable effects concentration (3 mg L?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 plants 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 mg L?1), the lowest
observable effects concentration (3 mg L?1) (Jones and Kerswell, 2003) and the locally-derived marine trigger value (75 mg L?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. GreatBarrierReefcatchmentarea,samplingsites,andplumetebuthiuronconcentrationcontours.TebuthiuronresiduesweredetectedoffshorefromtheBurdekinRiver(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 mg L?1), the locally-
derived marineecological protection trigger value (0.02mg L?1) (GBRMPA, 2008) and thelowestobservable effectsconcentration (10mg L?1) (Jones and Kerswell,2003).The contoursare
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 eventover
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
observable effects concentration: Haynes et al., 2000b) of diuron
were found in the river water plumes 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 for atrazine (GBRMPA, 2008) (Fig. 3) was
only exceeded offshore from the Pioneer River, although the
current lowest observable effect concentration (Jones and Ker-
swell, 2003) was not. Hexazinone residues (Fig. 4) were detectable
offshore from theTully 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 conform 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) 2470–24842481
(Mackay Whitsunday) but concentrations were well below any
known effects level (Jones and Kerswell, 2003) 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 samples exceeded the locally 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
tebuthiuron) measured in the GBR lagoon exceeded known effect
concentrations (Haynes et al., 2000b; Jones and Kerswell, 2003)
and/or locally derived ecological protection trigger values for the
GBR (GBRMPA, 2008) offshore from the mouths of the Tully,
Burdekin, O’Connell and Pioneer Rivers. While 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 due
to the combination 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-
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,
2003; 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 mg L?1) compared to Cymodocea serrulata (10 mg L?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
Loads of herbicides (kg) and event mean concentrations (EMC: mg L?1) exported from waterways.
West Barratta Creek2005/06
O’Connell River 2004/05
EMC: Event mean concentration.
BDL: No load calculated as concentrations were below the analytical limit of detection (0.01 mg L?1); þ No load calculated as only a single sample with concentration above
aMitchell et al., 2005.
S.E. Lewis et al. / Environmental Pollution 157 (2009) 2470–24842482
Herbicides mayact insynergy withotherchemicalpollutantsand
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.,
quantum yield) in these experiments have been recorded within
hours of exposure at levels as low as 0.1 mg L?1(Haynes et al.,
2000b), although most species recovered after the exposure ceased
(Haynes et al., 2000b; Jones, 2005; Jones and Kerswell, 2003; Jones
et al., 2003; Negriet 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., 2008).
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 mostexposed toland-
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.
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) laboratoryforanalysing the pesticide samples and
particularly Simon Christen (QHFSS) who provided additional
details on the analytical method.
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