Impacts of lawn-care pesticides on aquatic ecosystems in relation to

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Impacts of lawn-care pesticides on aquatic ecosystems
in relation to property value
Jay P. Overmyera,
,
, Raymond Nobleta and Kevin L. Armbrustb
a
University of Georgia, Department of Entomology, 413 Biological Sciences Building,
Athens, GA 30602, USA
b
Mississippi State Chemical Laboratory, PO Box CR, Mississippi State, MS 39762, USA
Received 20 August 2004; accepted 11 February 2005. Available online 24 May 2005.
Abstract
To determine the potential impacts of lawn-care pesticides on aquatic ecosystems, the
macroinvertebrate communities of six streams were assessed using a multimetric
approach. Four streams flowed through residential neighborhoods of Peachtree City, GA,
USA, with differing mean property values and two reference streams were outside the
city limits. A series of correlation analyses were conducted comparing stream rank from
water quality and physical stream parameters, habitat assessments, benthic
macroinvertebrate metric, pesticide toxicity and metal toxicity data to determine
relationships among these parameters. Significant correlations were detected between
individual analyses of stream rank for pesticide toxicity, specific conductance, turbidity,
temperature and dissolved oxygen with benthic macroinvertebrate metrics.
The macroinvertebrate communities of suburban streams may be influenced by the
toxicity of the pesticides present in the water and sediment as well as select water quality
parameters.
Keywords: Macroinvertebrates; Pesticides; Property value; Rapid bioassessment;
Suburban streams
Article Outline
1. Introduction
2. Study sites
3. Materials and methods
3.1. Habitat assessment
3.2. Water quality
3.3. Benthic sampling
3.4. Benthic metrics
3.5. Pesticide Toxicity Index
3.6. Chemical analysis
3.7. Data analysis
4. Results
4.1. Habitat assessment
4.2. Water quality
4.3. Pesticides
4.4. Macroinvertebrate assessment
5. Discussion
6. Conclusions
Acknowledgements
References
1. Introduction
Urban and suburban streams have the potential to be highly impacted by chemicals used
to protect lawns, ornamental plants, and home gardens from pests. An estimated 80
million pounds of pesticide-active ingredients are applied annually in domestic settings
for control of insects, invasive plants, weeds, and fungi on lawns and gardens (U.S.
Environmental Protection Agency, http://www.epa.gov/oppbead1/pestsales/99pestsales).
Lawn-care pesticides enter waterways primarily through runoff from rain events and are
commonly detected in these aquatic systems (USGS, 1999). Several chemicals, primarily
insecticides, have been detected at concentrations exceeding aquatic life criteria (USGS,
1999). Thus, organisms inhabiting urban and suburban streams may be adversely affected
by the presence of lawn-care pesticides.
Macroinvertebrates have been widely used to assess the effects of contaminants on
stream ecosystems in urban areas (Beasley and Kneale, 2002, Duda et al., 1982, Garie
and McIntosh, 1986 and Medeiros et al., 1983). Macroinvertebrates can be considered
excellent biomonitors of aquatic systems because they are ubiquitous, sedentary, exhibit a
range or responses to contaminants, and have relatively long lifecycles (Rosenberg and
Resh, 1996). In addition, macroinvertebrate indices such as the
Ephemeroptera + Plecoptera + Trichoptera (EPT) Index and the North Carolina Biotic
Index (NCBI) have been shown to track ecological processes in insecticide-treated
streams (Wallace et al., 1996) indicating that macroinvertebrate communities are
sensitive to pesticides and are good indicators of overall ecosystem function.
While many studies have been conducted assessing the effects of contaminants on
macroinvertebrate communities in urban streams, the contaminants of interest were
primarily metals and polycyclic aromatic hydrocarbons (PAHs) (Beasley and Kneale,
2002, Duda et al., 1982, Garie and McIntosh, 1986 and Medeiros et al., 1983) with no
mention of pesticides even though the highest concentrations of several pesticides have
been detected in urban streams (USGS, 1999). Thus, the impact of pesticides on
macroinvertebrate communities needs to be investigated in urbanized streams, especially
suburban streams which are subject to lawn-care pesticide runoff.
The objectives of this research were to determine the potential impact of lawn-care
pesticides on the macroinvertebrate communities of streams in a suburb of Atlanta, GA,
USA and to determine if impacts are related to the value of the property through which
the streams flow. The idea being that homes with higher property values typically have
well-manicured lawns. Thus, homeowners in high property value areas are likely to apply
more pesticides to their lawns than those with lesser-valued property. Six streams, four
flowing through residential neighborhoods in Peachtree City, GA, USA, with differing
mean property values and two references outside the city limits, were assessed using a
multimetric approach. Results of the multimetric analyses will be compared with a
Pesticide Toxicity Index (Munn and Gilliom, 2001) for each stream to determine any
relationship between impairment indicated by the multimetric indices and pesticide
toxicity.
2. Study sites
Peachtree City, GA, USA, is located in Fayette County, approximately 25 miles south of
Atlanta, GA, USA. All streams are located in the headwaters of the Upper Flint River
watershed in the Piedmont Ecoregion of Georgia. Four of the six streams assessed in this
study, Smoke Rise (N 33°0.07′; W 84°34.03′), Stoney Brook (N 33°25.61′; W 84°34.11′),
Oak Newel (N 33°23.11′; W 84°33.35′), and Cherry Branch (N 33°24.33′; W 84°35.38′)
are within the Peachtree City limits and receive runoff from residential lawns. The Smoke
Rise watershed has the highest mean property value ($388,900) followed by Stoney
Brook ($326,200), Cherry Branch ($187,000) and Oak Newel ($136,000). One of the
reference streams, Crabapple (N 33°27.00′; W 84°34.70′) was north of the city limits.
The other reference stream, Keg Creek (N 33°19.80′; W 84°34.58′) was located south of
the city limits in Coweta County. For a more complete description of the study sites and
property information see Herbert (2003).
3. Materials and methods
3.1. Habitat assessment
Prior to the first sampling period (Summer 2000), the habitats of the six streams were
assessed using the habitat assessment format for low gradient streams outlined in Barbour
et al. (1999). Scores from the 10 parameters were totaled for a cumulative habitat score.
In addition to the habitat assessment, median particle size of the stream substrate was
determined using the method of Wolman (1954).
3.2. Water quality
Water quality parameters were measured before each sampling period with a Hydrolab
datasonde®. Parameters measured were temperature, dissolved oxygen, pH, specific
conductance and turbidity. All measurements were made at the uppermost location of the
stream reach assessed.
3.3. Benthic sampling
Macroinvertebrate samples were collected quarterly over a two-year period beginning in
the Summer 2000 and ending in Spring 2002. Sampling of the six streams was conducted
on the same dates except for Summer 2000, Fall 2000 and Winter 2001 collections,
which were conducted within 48 h interval. Sampling was conducted with a 12-inch
diameter D-frame net with a 500 μm mesh using the multihabitat approach described by
Barbour et al. (1999). All samples were preserved in 95% ethanol and transported to the
lab for sorting. Samples were sorted by hand in white enamel pans. All invertebrates
collected were preserved in 70% ethanol and identified to genus or the lowest taxonomic
level possible using keys by Merritt and Cummins (1996) and Brigham et al. (1982).
3.4. Benthic metrics
Ten benthic metrics were used to assess the macroinvertebrate data. Metrics chosen
represented various measure categories (Barbour et al., 1999). The metrics used, along
with their category and predicted response to perturbation, are listed in Table 1.
Calculations and tolerance values for the North Carolina Biotic Index (NCBI) and the
Biotic Condition Index (BCI) can be found in Lenat (1993) and Winget and Mangum
(1979), respectively. For the NCBI calculations in this study, the denominator in the
equation was total abundance. Genus tolerance values for taxa with several species were
established by taking the average of all the tolerance values listed for that genus.
Table 1.
Benthic metrics used in the assessment of macroinvertebrate data and the predicted response of the metric
to increasing perturbation
Category
Metric
Predicted response
Richness measures
Total # taxa
Decrease
# EPT taxa
Decrease
% EPT
Decrease
% Chironomidae
Increase
% Dominant taxon
Increase
North Carolina Biotic Index (NCBI)
Increase
Biotic Condition Index (BCI)
Decrease
Composition measures
Tolerance measures
Category
Metric
Predicted response
Feeding measures
% Scrapers
Decrease
% Shredders
Decrease
% Clingers
Decrease
Habit measures
3.5. Pesticide Toxicity Index
The Pesticide Toxicity Index (PTI) (Munn and Gilliom, 2001) was used to rank the level
of contamination in the streams based on the concentrations and relative toxicities of the
pesticides detected from monthly water and sediment samples. The PTI score was
calculated by the following equation:
where Ei = concentration of pesticide i in water or sediment, MTCx,i = median toxicity
concentration for the pesticide i for taxonomic group x, and n = number of pesticides.
The PTI scores for each stream in this study were determined by adding the PTI value
calculated from pesticide concentrations in water with the PTI value calculated from
pesticides' concentrations in the sediment. For the water PTI value, average pesticide
concentrations measured from monthly water samples were used with 48 h EC50 data for
Daphnia magna. For the sediment PTI value, average pesticide concentrations measured
from monthly sediment samples were used with 48 h LC50 data for Chironomus tentans
determined in sediment toxicity tests. If sediment toxicity data for C. tentans were not
available for a particular pesticide, a ratio of the EC50 for D. magna to the LC50 for C.
tentans for chlorpyrifos was used to determine a relative LC50 for the pesticide.
Although we realize that there will be error associated with this method, the toxicity will
be more representative of sediments which typically bind pesticides making them less
bioavailable and consequently less toxic than pesticides dissolved in water (Suedel et al.,
1996). All PTI scores reported were multiplied by 1 × 103.
3.6. Chemical analysis
At each site, water and sediment samples were collected to determine concentrations of
pesticides present at these sites. Water samples were collected into 1 L amber glass
bottles with Teflon lids and sediment samples were collected into 1-quart glass mason
jars. All samples were immediately placed into ice-chests and transported on ice to the
laboratory where they were stored frozen at −20 °C until analysis. Pesticides were
extracted from water samples by acidifying a 500-ml aliquot to pH < 2 with concentrated
hydrochloric acid and drawing it under vacuum through a C-18 solid-phase extraction
cartridge. Pesticides were eluted from the cartridge with 3 ml of a 2:1 (v/v) mixture of
ethyl acetate and diethyl ether. Acidic pesticides in the extract were esterified with 2 ml
of etheryl diazomethane and the final volume of the extract was reduced to 2 ml under a
stream of nitrogen. Pesticides in 50 g sediment samples were sequentially extracted with
50-ml aliquots of ethyl acetate and 40 ml of a 3:1 mixture of ethyl acetate and ammonium
acetate, respectively. The extracts were pooled and excess water was removed with a
seperatory funnel. The final extract volume was recorded and a 3 ml aliquot was treated
with diazomethane as described above. Pesticides' residues in sample extracts were
analyzed by gas chromatography–mass spectrometry (GC–MS) using chemical ionization
operating in the negative ion mode. Limits of quantitation for pesticides in water were set
at 0.1 ng/L while those in sediment were set at 0.1 μg/kg.
3.7. Data analysis
Benthic metrics were analyzed for normality and homoscedasticity using Shapiro-Wilk's
and Bartlett's tests, respectively. Metrics with percentage data were arcsine square root
transformed and the EPT taxa richness metric was square root transformed before
analysis. The only metric that failed to meet the normality and homoscedasticity
requirements, even after data transformations, was % shredders. Thus, this metric was
removed from the analysis. The remaining nine metrics were analyzed using an Analysis
of Variance (ANOVA) random effects model. The random effects model was used
because of the lack of independence in the data or pseudoreplication of samples from the
same streams over time. Specific differences among streams for each metric were
analyzed with a Tukey's studentized range test. The pesticide data and water quality data
were analyzed with a non-parametric Kruskal–Wallis test to determine differences among
streams. Specific differences were determined using a Newman–Kuels multiple
comparisons test (Zar, 1999). Relationships among pesticide toxicity, habitat quality and
physical stream parameters with benthic macroinvertebrate metric data were analyzed
using a Kendall's rank correlation test (Sokal and Rohlf, 1995).
4. Results
4.1. Habitat assessment
Smoke Rise had the best habitat of the six streams assessed with a cumulative score of
144. The habitats at Stoney Brook, Keg Creek and Oak Newel were similar to Smoke
Rise with cumulative scores of 141, 140, and 136, respectively. The Crabapple and
Cherry Branch sites scored considerably lower with cumulative scores of 124 and 107,
respectively. Although Crabapple was designated as one of the reference sites because of
its location (forested rural area outside the city limits), this site scored marginal in pool
variability, pool substrate composition and channel flow and poor in sediment deposition.
Cherry Branch scored marginal in epifaunal substrate, pool substrate composition,
channel alteration, and channel sinuosity; it scored poor in pool variability and sediment
deposition. Stoney Brook was the stream with the largest median particle size (8 mm).
The remaining five streams all had median particle sizes <1 mm. Analyzing only the
particles measured >1 mm, Stoney Brook had the largest median size (150 mm) followed
by Smoke Rise (56 mm), Oak Newel (55 mm), Cherry Branch (23 mm), Crabapple
(16 mm) and Keg Creek (<1 mm).
4.2. Water quality
Analysis of the water quality data showed that there were significant differences in
specific conductance (p = 0.0120), pH (p = 0.0354) and turbidity (p = 0.0036) among
streams (Table 2). Specific conductance was significantly different at all sites except
Smoke Rise and Oak Newel which were statistically similar. Oak Newel had a
statistically higher pH (6.7 ± 0.2) than the other five sites; the pH value at Stoney Brook
was statistically lower (6.1 ± 0.2) than the others. The pH values at Cherry Branch and
Keg Creek were statistically similar as was the pH at Crabapple and Smoke Rise.
Turbidity was statistically similar at Cherry Branch, Oak Newel and Crabapple but
statistically different at Keg Creek, Stoney Brook and Smoke Rise.
Table 2.
Mean values ± standard deviation (n = 8) for water quality parameters measured in the six streams
Site
Temperature
(°C)
Dissolved
oxygen (mg/L)
pH
Specific
conductance
(μS/cm)
Turbidity
(NTU)
Oak Newel
15.2 ± 4.6a
8.8 ± 1.5a
6.7 ± 0.2a
60.0 ± 4.7b
8.2 ± 4.2c
Keg Creek
14.6 ± 5.8a
8.9 ± 2.0a
6.5 ± 0.2b
55.4 ± 4.5c
15.2 ± 3.8a
Stoney Brook
15.8 ± 5.4a
8.7 ± 1.7a
6.1 ± 0.2d
44.5 ± 1.8e
10.2 ± 4.3b
Crabapple
15.3 ± 5.8a
8.8 ± 1.5a
6.3 ± 0.3c
52.6 ± 9.9d
11.8 ± 14.4c
Smoke Rise
15.7 ± 4.4a
8.4 ± 1.1a
6.3 ± 0.2c
60.7 ± 6.7b
4.5 ± 1.2d
Cherry Branch
16.9 ± 5.5a
8.7 ± 1.1a
6.5 ± 0.2b
70.2 ± 6.8a
9.3 ± 5.0c
Means with different letters are significantly different as determined by a non-parametric Newman–Keuls
multiple comparisons test (p < 0.05).
4.3. Pesticides
Nine pesticides (3 insecticides, 4 herbicides and 2 fungicides) were detected in water
samples taken from the streams (Table 3). All pesticides were detected in each stream
except for malathion at Oak Newel and diazinon at Keg Creek and Stoney Brook. No
significant differences in concentrations of the nine pesticides were observed among
streams (p > 0.10). This indicates that although our reference streams were in rural areas
away from neighborhoods, they were still susceptible to pesticide contamination from
upstream sources. The most frequently detected pesticides were dithiopyr, chlorothalonil
and chlorpyrifos which were detected in 78%, 69% and 53% of the samples, respectively.
The remaining pesticides were detected in <30% of the samples. Dithiopyr was the
pesticide detected at the highest concentration in all streams with averages ranging
between 12.72 ng/L at Stoney Brook and 22.60 ng/L at Crabapple.
Table 3.
Pesticides detected in water samples from the six streams between Summer 2000 and Spring 2002
Site
Oak Newel
Keg Creek
Stoney Brook
Pesticides detected
% Detectiona
Concentration (ng/L)
Max
Meane
Chlorpyrifosb
50
5.22
0.48
Diazinonb
5
6.28
0.29
Dithiopyrc
81
122.68
14.29
Pendimethalinc
14
0.77
0.07
Oxadiazonc
36
25.14
1.78
Chlorothalonild
64
13.40
1.50
Flutolanild
18
42.32
3.08
Chlorpyrifos
57
5.27
0.52
Malathion
13
0.95
0.09
Dithiopyr
71
252.50
21.75
Pendimethalin
9
0.90
0.06
Oxadiazon
35
57.82
3.49
Chlorothalonil
65
171.91
8.06
Flutolanil
12
288.05
17.21
Chlorpyrifos
43
4.77
0.41
Malathionb
9
3.53
0.18
Dithiopyr
76
142.92
12.72
Pendimethalin
9
1.32
0.11
Oxadiazon
26
24.75
1.36
Chlorothalonil
70
8.21
0.70
Site
Crabapple
Smoke Rise
Cherry Branch
Pesticides detected
% Detectiona
Concentration (ng/L)
Max
Meane
Flutolanil
6
65.50
3.85
Chlorpyrifos
55
8.00
0.82
Diazinon
5
1.43
0.07
Malathion
9
0.57
0.05
Dithiopyr
81
243.43
22.60
Pendimethalin
14
5.74
0.36
Prodiaminec
5
2.09
0.10
Oxadiazon
36
5.39
0.41
Chlorothalonil
68
74.13
4.12
Flutolanil
19
28.84
1.97
Chlorpyrifos
57
6.44
0.51
Diazinon
4
1.38
0.06
Malathion
4
0.80
0.03
Dithiopyr
76
184.56
16.59
Pendimethalin
26
1.84
0.23
Prodiamine
4
1.89
0.08
Oxadiazon
13
2.43
0.20
Chlorothalonil
70
21.57
1.84
Flutolanil
12
10.46
1.22
Chlorpyrifos
57
7.43
0.78
Diazinon
13
18.32
0.94
Malathion
13
11.53
0.65
Dithiopyr
82
179.58
21.44
Pendimethalin
26
12.02
0.81
Site
Pesticides detected
% Detectiona
Concentration (ng/L)
Max
Meane
Prodiamine
13
7.40
0.46
Oxadiazon
39
38.86
2.16
Chlorothalonil
74
30.05
2.38
Flutolanil
12
44.93
2.75
a
% of samples the pesticide was detected above the level of quantification.
Insecticide.
c
Herbicide.
d
Fungicide.
e
Mean concentrations were calculated by taking an average of the concentrations from all sampling dates.
Pesticide concentrations below the level of quatitation were considered to be 0.
b
Six pesticides (2 insecticides, 3 herbicides and 1 fungicide) were detected in sediment
samples (Table 4). Dithiopyr and chlorpyrifos were the only two pesticides detected in
the sediments of all six streams. Chlorpyrifos was detected in 54% of the samples and
dithiopyr was detected in 40% of the samples collected. Dithiopyr was the pesticide
detected at the highest concentration in all streams with averages ranging between
2.89 μg/L at Keg Creek and 0.61 μg/L at Crabapple. Concentrations of pesticides in the
sediments were not significantly different among streams (p > 0.10).
Table 4.
Pesticides detected in sediment samples from the six streams between Summer 2000 and Spring 2002
Site
Oak Newel
Keg Creek
Stoney Brook
Pesticides detected
% detectiona
Concentration (μg/L)
Max
Meane
Chlorpyrifosb
47
0.56
0.15
Diazinonb
7
0.66
0.04
Dithiopyrc
40
25.88
2.30
Chlorothalonild
7
1.09
0.07
Chlorpyrifos
60
0.69
0.22
Dithiopyr
40
33.86
2.89
Chlorpyrifos
53
3.87
0.37
Site
Crabapple
Smoke Rise
Cherry Branch
Pesticides detected
% detectiona
Concentration (μg/L)
Max
Meane
Diazinon
7
0.94
0.06
Dithiopyr
40
3.92
0.72
Oxadiazonc
7
0.21
0.01
Chlorothalonil
7
0.55
0.04
Chlorpyrifos
53
0.59
0.17
Dithiopyr
40
1.91
0.61
Pendimethalinc
7
0.36
0.02
Chlorothalonil
7
0.91
0.06
Chlorpyrifos
53
0.29
0.10
Diazinon
7
0.97
0.06
Dithiopyr
40
5.04
0.92
Chlorothalonil
7
0.20
0.01
Chlorpyrifos
60
0.48
0.17
Dithiopyr
40
36.79
2.84
Chlorothalonil
7
0.69
0.05
a
% of samples the pesticide was detected above the level of quantification.
Insecticide.
c
Herbicide.
d
Fungicide.
e
Mean concentrations were calculated by taking an average of the concentrations from all sampling dates.
Pesticide concentrations below the level of quatitation were considered to be 0.
b
Measurement of the toxicity of the pesticides in the streams through summation of the
PTI values calculated from cumulative water and sediment data indicated that Cherry
Branch was the most toxic (PTI = 3.56) followed by Crabapple (PTI = 2.62), Stoney
Brook (PTI = 2.15), Keg Creek (PTI = 2.01), Oak Newel (PTI = 1.88), and Smoke Rise
(PTI = 1.64).
4.4. Macroinvertebrate assessment
A total of 66 families and 108 genera of macroinvertebrates were collected in the streams
assessed in this study. Chironomids were the most abundant taxa in all streams
comprising as high as 76.7% of the total abundance at Cherry Branch. Average
abundance ranged from 145 macroinvertebrates/sample at Cherry Branch to 897
macroinvertebrates/sample at Oak Newel. Taxa commonly collected throughout the study
with their respective percentage abundance are listed in Table 5.
Table 5.
Taxa present in ≥50% of samples collected from each stream (n = 8) reported as percentage of total
abundance
Taxon
Oak (%)
Keg (%)
Stoney (%)
Crab (%)
Smoke (%)
Cherry (%)
Chironomidae
29
30
55
45
60
77
Anchytarsus spp.
13
Leuctra spp.
10
Habrophlebiodes spp.
8
Diplectrona spp.
8
Stenonema spp.
8
1
1
2
11
14
8
15
Baetis spp.
5
3
5
Cheumatopsyche spp.
4
<1
3
Chimarra spp.
4
<1
Limnophila spp.
4
<1
Isoperla spp.
<1
<1
2
Stenelmis spp.
3
Lepidostoma spp.
3
Tipula spp.
2
4
<1
2
Hydropsyche spp.
1
1
4
1
Simulium spp.
1
2
4
<1
<1
3
<1
1
Hexagenia spp.
3
Perlesta spp.
3
Procambarus spp.
2
1
3
1
1
2
2
8
1
3
3
2
1
2
Taxon
Oak (%)
Keg (%)
Stoney (%)
Crab (%)
Gomphus spp.
3
1
Macronychus spp.
2
1
Hygrotus spp.
2
2
Hemerodromia spp.
1
1
<1
1
Rhagovelia spp.
1
1
1
2
Calopteryx spp.
1
<1
<1
1
Nigronia spp.
<1
1
Bezzia spp.
<1
<1
<1
Progomphus spp.
1
Argia spp.
1
Ancyronyx spp.
1
Dineutus spp.
1
Serretella spp.
1
Baetisca spp.
1
Pycnopsyche spp.
1
Corbicula spp.
1
Hexatoma spp.
<1
2
Chrysops spp.
<1
1
Lype spp.
<1
Sialis spp.
<1
Boyeria spp.
<1
Cherry (%)
2
2
1
<1
1
2
1
2
<1%
Polycentropus spp.
Smoke (%)
<1
Dicranota spp.
<1
Ectopria spp.
<1
Psilotreta spp.
<1
Taxon
Oak (%)
Keg (%)
Stoney (%)
Dixa spp.
<1
Lanthus spp.
<1
Cordulegaster spp.
<1
Dixella spp.
Crab (%)
Smoke (%)
Cherry (%)
<1
<1
<1
Clinocera spp.
<1
From the scores obtained in the 10 benthic macroinvertebrate metrics, the streams were
ranked from highest to lowest biotic integrity. The Oak Newel site ranked highest,
scoring best in 44% of the metrics used in the analysis followed by Keg Creek (22%),
Stoney Brook (22%), Crabapple (11%), Smoke Rise (0%) and Cherry Branch (0%)
(Table 6). All Keg Creek metric scores were statistically similar (p > 0.05) to both Stoney
Brook and Crabapple scores while Stoney Brook and Crabapple differed in only one
metric. These three sites were statistically similar to Oak Newel in ≥78% of the metrics.
The Smoke Rise site appears to be slightly impaired, scoring significantly similar in only
33% of the metrics with Oak Newel and Keg Creek. However, Smoke Rise scored
significantly similar to Crabapple and Stoney Brook in 78% and 67% of the metrics,
respectively. The Cherry Branch site was the most impaired, scoring significantly similar
in ≤22% of the metrics with all sites except Smoke Rise, which was significantly similar
to Cherry Branch in 89% of the metrics assessed.
Table 6.
Mean scores ± standard deviation (n = 8) of benthic metrics calculated from quarterly sampled
macroinvertebrate data for the six study sites
Benthic metric
Site
Score
Total # taxa
Oak Newel
22.3 ± 7.0a,b
Keg Creek
29.0 ± 6.3a
Stoney Brook
28.8 ± 5.1a
Crabapple
24.3 ± 4.6a
Smoke Rise
15.1 ± 5.3b,c
Cherry Branch
12.5 ± 3.9c
Oak Newel
7.8 ± 3.3a
# EPT taxa
Benthic metric
% EPT
% Chironomidae
NCBI
BCI
Site
Score
Keg Creek
11.1 ± 4.7a
Stoney Brook
11.6 ± 2.3a
Crabapple
7.3 ± 1.6a,b
Smoke Rise
4.1 ± 2.3b,c
Cherry Branch
3.6 ± 1.9c
Oak Newel
44.3 ± 11.6a
Keg Creek
37.9 ± 14.3a
Stoney Brook
30.6 ± 15.3a,b
Crabapple
35.0 ± 16.9a,b
Smoke Rise
32.9 ± 6.1b,c
Cherry Branch
6.5 ± 11.4c
Oak Newel
25.8 ± 8.8a
Keg Creek
34.4 ± 20.1a,b
Stoney Brook
49.1 ± 19.5b,c
Crabapple
40.6 ± 17.8a,b
Smoke Rise
63.9 ± 21.3b,c
Cherry Branch
76.1 ± 26.9c
Oak Newel
4.30 ± 0.52a
Keg Creek
5.25 ± 0.44b,c
Stoney Brook
5.03 ± 0.59a,b
Crabapple
5.34 ± 0.71b,c
Smoke Rise
5.27 ± 0.25b,c
Cherry Branch
5.93 ± 0.44c
Oak Newel
91.0 ± 7.4a,b,*
Keg Creek
86.8 ± 7.8a,b
Stoney Brook
93.8 ± 6.1a
Benthic metric
% Dominant taxon
% Scrapers
% Clingers
Site
Score
Crabapple
83.0 ± 3.4b
Smoke Rise
86.8 ± 3.6a,b
Cherry Branch
71.1 ± 3.9c
Oak Newel
32.9 ± 9.1b
Keg Creek
31.4 ± 17.8a
Stoney Brook
50.9 ± 17.4b,c
Crabapple
42.7 ± 12.9b
Smoke Rise
61.4 ± 21.3b,c
Cherry Branch
73.6 ± 24.9c
Oak Newel
19.6 ± 7.9a
Keg Creek
18.3 ± 9.5a
Stoney Brook
17.2 ± 9.6a
Crabapple
20.0 ± 10.7a
Smoke Rise
3.3 ± 1.8b
Cherry Branch
1.0 ± 3.4b
Oak Newel
65.8 ± 11.6a
Keg Creek
41.8 ± 13.0b
Stoney Brook
36.2 ± 10.6b,c
Crabapple
39.6 ± 14.7b,c
Smoke Rise
19.9 ± 10.5c,d
Cherry Branch
20.0 ± 14.8d
*Means with different letters are significantly different as determine by Tukey's studentized range test
(p < 0.05).
Because our reference streams did not have the highest overall metric ranks and the PTI
scores were higher than some of the sites draining residential neighborhoods in this study,
alternative reference stream data for the Piedmont ecoregion of Georgia, USA, were
sought. A study by Hughes et al. (2004, unpublished data) assessed several streams
throughout the state of Georgia, USA, to develop reference conditions for each ecoregion
(D.L. Hughes, personal communication). The method and study design for collecting
macroinvertebrates was identical to our study, and many of the same metrics were used
for analysis of the data. In comparison of results obtained from our study and those from
Hughes et al. (2004, unpublished data), the Oak Newel and Keg Creek sites scored within
the range of the reference streams in five of the seven metrics similar to both studies. The
Stoney Brook and Crabapple sites scored within the range of the reference streams in
only three and two metrics, respectively. The Smoke Rise and Cherry Branch sites did
not score within the range of the reference streams in any metric. Based on comparison of
these two studies, it appears that the Oak Newel, Keg Creek and Stoney Brook sites are in
good to fair condition, the Crabapple site is fair to slightly impaired and the Smoke Rise
and Cherry Branch sites are impaired.
To determine the relationship among pesticide toxicity, water quality, habitat quality and
physical stream parameters with macroinvertebrate metric data, a series of comparisons
were conducted using ranked data. The macroinvertebrate metric data were significantly
correlated with stream rank from the pesticide toxicity data (τ = 1.31, n = 6, p < 0.05).
Increased biotic integrity as determined by the macroinvertebrate metric data was
significantly correlated with a decrease in specific conductance (τ = 0.94, n = 6,
p < 0.05), an increase in turbidity (τ = −0.94, n = 6, p < 0.05), a decrease in temperature
(τ = 1.69, n = 6, p < 0.05) and an increase in dissolved oxygen (τ = −1.69, n = 6,
p < 0.05). However, the pH of the streams was not significantly correlated with the
macroinvertebrate metric data (τ = −0.56, n = 6, p < 0.05). Stream rank from the
macroinvertebrate metric data was not significantly correlated with stream habitat
(τ = −0.56, n = 6, p > 0.05), depth (τ = −0.56, n = 6, p > 0.05), velocity (τ = −0.56, n = 6,
p > 0.05) or median particle size (>1 mm) (τ = 0.19, n = 6, p > 0.05).
Because there was a significant correlation between pesticide toxicity and the benthic
metric data, additional rank correlation tests were conducted to determine which metrics
varied similarly to the PTI data. Of the nine metrics used in this study, five had stream
rank significantly correlated with PTI rank. The NCBI metric produced the greatest
correlation between stream rank and PTI rank (τ = 2.07, n = 6, p < 0.05) followed by the
BCI (τ = −1.31, n = 6, p < 0.05). The % Chironomidae and % Clinger metrics produced
statistically similar correlations with the PTI stream ranks (τ = 0.94, n = 6, p < 0.05); the
% EPT metric was significantly negatively correlated with PTI stream ranks (τ = −0.94,
n = 6, p < 0.05).
Because there were data from year 1 of this study for concentrations of the metals copper,
arsenic and zinc from sediments (L.M. Shuman, unpublished data), we were interested in
determining if metal toxicity (calculated similarly to the PTI) was related to the
macroinvertebrate metric data for year 1. The rank correlation analysis indicated that
there was no significant correlation between the two variables (τ = 0.56, n = 6, p > 0.05).
To determine relationships between the property value of the watersheds surrounding the
streams with the biotic integrity of the stream determined by the macroinvertebrate metric
data and the pesticide toxicity data, similar ranked correlations were conducted. There
was no significant correlation between property value and the macroinvertebrate metric
data (τ = 0.56, n = 6, p > 0.05), or property value and pesticide toxicity (τ = −0.56, n = 6,
p > 0.05).
5. Discussion
The habitats of the six streams assessed in this study were similar except for the
Crabapple and Cherry Branch sites which scored marginal or poor in several categories.
All the streams were affected by sedimentation to some extent. Median particle size was
<1 mm for all streams except Stoney Brook; however, 45% of the particles at Stoney
Brook were also <1 mm. The addition of sediments to these streams is likely due to past
agricultural practices in the area considering that the riparian zones of all the streams
were extensive and well established.
There were significant differences detected for three of the water quality parameters
measured in the six streams. Two of which, specific conductance and turbidity, were
significantly correlated with the macroinvertebrate metric data. Specific conductance and
turbidity have been shown to affect macroinvertebrate populations in other studies.
Specific conductance was negatively correlated with biotic integrity in a study conducted
by Roy et al. (2003a). Lloyd et al. (1987) showed that reductions in macroinvertebrate
density and biomass were significantly correlated with increased turbidity. However, in
this study, increased biotic integrity was associated with an increase in turbidity as
opposed to a decrease in turbidity. Increases in suspended solids and organic matter have
been shown to decrease the bioavailability of organic chemicals (Hall et al., 1986 and
Kadlec and Benson, 1995). Thus, it is possible that an increase in turbidity made some of
the chemicals present in the water less available for uptake by the macroinvertebrates,
decreasing their potential toxicity.
Two parameters not significantly different among streams, temperature and dissolved
oxygen, were also significantly correlated with the macroinvertebrate metric data.
However, some of the smaller streams in this study tend to warm and cool over the
course of the day, especially in the Spring and Fall. Hourly temperature data recorded at
Oak Newel showed temperature to fluctuate by as much as 5 °C (S. Herbert, unpublished
data). Thus, measuring the temperature in a stream sampled in early morning may not
likely be the same if measured in late afternoon. Mean daily temperatures were
significantly different among these streams in a study conducted by Herbert (2003).
Consequently, the time of the sampling could have confounded the significance of
temperature among streams. Likewise, dissolved oxygen is related to water temperature
and could also have been confounded by the time of sampling.
The PTI was developed to evaluate the relative risk of pesticides to aquatic organisms in
streams (Munn and Gilliom, 2001). Although this index is useful for ranking streams
based on expected toxicity, it is not a direct measure of toxicity to biological
communities because factors such as bioavailability and synergistic chemical interactions
are not accounted for (Munn and Gilliom, 2001). However, the index is more biologically
relevant than ranking streams on measured pesticide concentration because not all
pesticides are equally toxic. Thus, high concentrations of a relatively non-toxic herbicide
will not overestimate the toxicity of the stream.
In this study, the PTI was used to rank the six streams assessed based on their expected
toxicity to macroinvertebrates to determine if macroinvertebrate community structure is
related to the presence of lawn-care pesticides. Results showed that the two variables
were significantly correlated indicating that as pesticide toxicity increases in the streams,
the macroinvertebrate communities become increasingly stressed as indicated by the
macroinvertebrate metrics. Although physical stream parameters such as depth, velocity,
substrate size (Erman and Erman, 1984, Gore et al., 2001, Minshall, 1981 and Statzner,
1981) and habitat (Roy et al., 2003b) have been shown to affect macroinvertebrate
communities, none of these parameters were significantly correlated with the overall
macroinvertebrate metric data. However, a ranked comparison of median particle size
with each metric individually showed that there was a significant correlation between
particle size and the BCI. Calculation of tolerance values for the BCI takes into
consideration substrate preference and is considered to be a sensitive index for
determining the effects of sedimentation (Barbour et al., 1999). Thus, when comparing
rank particle size with the overall metric ranks for the streams, this relationship may have
been masked by the results of metrics that do not account for tolerance to sediments.
Consequently, substrate size may also be related to macroinvertebrate community
structure.
The only site that appeared to be an outlier in the correlation analysis between ranked PTI
and metric data was Smoke Rise. This site had the lowest PTI score but was the second
most impaired stream assessed in this study based on scores from the macroinvertebrate
metrics. Smoke Rise also had the highest habitat ranking and marginal sedimentation
compared to the other six streams assessed. A possible reason for the impairment
detected at Smoke Rise may be metal contamination. Smoke Rise had the highest
potential for metal toxicity of the six streams based on the metal toxicity index. In
addition, concentrations of copper, arsenic and zinc in the sediments during year 1 of this
study were on average approximately 3.6, 2.5 and 1.3 times higher, respectively, at
Smoke Rise than the other sites (L.M. Shuman, unpublished data). However, the
concentrations measured were well below toxic thresholds for the respective metals, so
expected effects on aquatic life would be minimal (US EPA, 2002). Thus, it is quite
possible that contaminant(s) or physical parameter(s) not measured in this study may be
affecting the benthic community at Smoke Rise.
Pesticide concentrations measured in the six streams assessed in this study were low in
both water (ng/L) and sediment (μg/L). Thus, we would not expect to see detrimental
effects on the aquatic biota related to pesticide exposure considering that concentrations
of chlorpyrifos, diazinon, and malathion, the three most acutely toxic chemicals detected
in the water samples, were below aquatic life criteria concentrations (IJC, 1977, Larson et
al., 1999 and US EPA, 1991). However, these criteria do not take into account possible
synergistic or additive effects due to exposure to multiple pesticides, metals or other
contaminants (Larson et al., 1999). In addition, the toxicities of many of the degradation
products of these pesticides are not well known, which could add to the overall toxicity of
the stream (Larson et al., 1999).
The two most prevalent pesticides detected in the six streams were the herbicide
dithiopyr and the fungicide chlorothalonil. Dithiopyr is the active ingredient in several
“weed and feed” products for control of unwanted grasses especially crabgrass. It is
typically applied in the Spring and early Summer before the unwanted grasses emerge as
part of many lawn-care programs in Georgia (http://www.griffin.peachnet.edu/ggarden).
Chlorothalonil is typically applied to lawns for control of brown patch and dollar spot
diseases. Although it is not widely used on lawns for control of fungal diseases,
chlorothalonil is also present in other products such as paints and deck stains that are
used around homes and can contribute to the overall runoff into streams. Both dithiopyr
and chlorothalonil are highly water soluble, which makes them susceptible to runoff.
They are also stable in the environment, which explains their presence in water and
sediments throughout the year.
There was no relationship between the mean property values of the watersheds and the
ecological integrity of the streams draining these watersheds as determined by the
macroinvertebrate metric data. This is likely related to the fact that there was no
significant difference in the concentrations or types of pesticides detected among the six
streams and the PTI scores were not as high in the high property value watersheds
(Smoke Rise and Stoney Brook) as one of the reference streams (Crabapple) and a lower
property value watershed (Cherry Branch). Thus, it does not appear that homeowners in
the high property value neighborhoods are applying any more pesticides or have any
more of an impact on streams in their neighborhoods than those in lower property
neighborhoods or rural areas.
The two tolerance measure indices, the NCBI and the BCI, provided the best relationship
between the macroinvertebrate data and the pesticide toxicity data. While the NCBI has
been shown to be useful in assessing the effects of pesticides on stream ecosystems
(Wallace et al., 1996), the BCI is more useful for predicting the effects of physical
parameters (gradient and substrate) with select water quality parameters (alkalinity and
sulfate concentration) (Winget and Mangum, 1979). Although the BCI was developed for
use in Western streams, it was selected for use in this study because of its sensitivity for
sedimentation (Barbour et al., 1999). However, it appears that this index may be useful in
predicting chemical contamination as well.
Chironomids were the dominant taxa in all six streams assessed. With the exception of
Stoney Brook, % chironomid abundance increased with increasing impairment. This is
consistent with the expected response of the chironomid community to increased
impairment (Table 1). Chironomids are often found in high abundances in impaired
streams due to their ability to utilize multiple habitats, short life cycles, rapid
reproduction and tolerance to both metals and pesticides (Coffman and Ferrington, 1996,
Gower et al., 1994, Richardson and Kiffney, 2000, Ruse et al., 2000 and Stuijfzand et al.,
2000). Larvae of the beetle Anchytarsus spp., nymphs of the stonefly Leuctra spp. and
nymphs of the mayfly Habrophlebiodes spp. appeared to be good bioindicators of stream
quality for this study because they were frequently collected from the top one, two and/or
three ranked streams, comprised >5% of the total abundance in the top ranked stream
(Oak Newel) and are considered sensitive to pollution (Barbour et al., 1999 and Lenat,
1993). Although Anchytarsus spp. was also collected in the three lowest ranked streams
and Leuctra spp. was collected at Smoke Rise, the frequency of collection and abundance
of these taxa were lower.
6. Conclusions
Increased impairment of the six streams assessed in this study as determined by the
macroinvertebrate metric data was shown to be significantly correlated to increases in
pesticide toxicity and select water quality parameters. Physical stream parameters such as
depth, velocity, median particle size as well as habitat and other contaminants such as
metals were not significantly related to the overall macroinvertebrate metric data.
Although a positive relationship was observed between the macroinvertebrate indices and
the Pesticide Toxicity Index, effects due to unmeasured physical parameters and/or
pollutants on the macroinvertebrate community could be contributing to the effects
observed. There was also no correlation between property value and effects on the
macroinvertebrate community in the streams of Peachtree City, GA. This indicates that
lawn-care practices of homeowners in high property value neighborhoods are not
impacting aquatic systems any more than those in lower property value neighborhoods.
Continued monitoring of urban and suburban streams for pesticides along with
macroinvertebrate assessments in additional communities and watersheds will strengthen
our understanding of the relationships between pesticides and their effects on aquatic
organisms.
Acknowledgements
The authors would like to thank Tara Brandt, Chris Ryan, and Marianne Stephens for
help with macroinvertebrate sample processing, Erica Kratzer for help with
identifications and Nehru Mantripragada for help with the pesticide sample preparations
and analyses. We would also like to thank Sue Herbert, Duncan Hughes and Larry
Shuman for providing additional data for comparisons. This research has been supported
by a grant (R82-8007) from the U.S. Environmental Protection Agency's Science to
Achieve Results (STAR) program. Although the research described in the article was
funded by the U.S. Environmental Protection Agency's STAR program, it has not been
subjected to any EPA review and therefore does not necessarily reflect the views of the
Agency and no official endorsement should be inferred.
References
Barbour et al., 1999 M.T. Barbour, J. Gerritsen, B.D. Snyder and J.B. Stribling, Rapid
Bioassessment Protocols for use in Streams and Wadeable Rivers: Periphyton, Benthic
Macroinvertebrates and Fish (second ed.), U.S. Environmental Protection Agency, Office
of Water, Washington, DC, USA (1999) (EPA 841-B-99-002).
Beasley and Kneale, 2002 G. Beasley and P. Kneale, Reviewing the impact of metals and
PAHs on macroinvertebrates in urban watercourses, Progress in Physical Geography 26
(2002), pp. 236–270. Abstract-GEOBASE | Order Document | Full Text via CrossRef
Brigham et al., 1982 A.R. Brigham, W.U. Brigham and A. Gnilka, Aquatic Insects and
Oligochaetes of North and South Carolina, Midwest Aquatic Enterprises, Mahomet, IL,
USA (1982).
Coffman and Ferrington, 1996 W.P. Coffman and L.C. Ferrington Jr., Chironomidae. In:
R.W. Merritt and K.W. Cummins, Editors, Introduction to the Aquatic Insects of North
America, Kendall/Hunt, Dubuque, IA, USA (1996), pp. 635–754.
Duda et al., 1982 A.M. Duda, D.R. Lenat and D.L. Penrose, Water quality in urban
streams – what we can expect, Journal of the Water Pollution Control Federation 54
(1982), pp. 1139–1147. Abstract-Compendex | Abstract-Compendex | Abstract-EMBASE
| Order Document
Erman and Erman, 1984 D.C. Erman and N.A. Erman, The response of stream
macroinvertebrates to substrate size and heterogeneity, Hydrobiologia 108 (1984), pp.
75–82. Abstract-GEOBASE | Order Document | Full Text via CrossRef
Garie and McIntosh, 1986 H.L. Garie and A. McIntosh, Distribution of benthic
macroinvertebrates in a stream exposed to urban runoff, Water Resources Bulletin 22
(1986), pp. 447–456.
Gore et al., 2001 J.A. Gore, J.B. Layzer and J. Mead, Macroinvertebrate instream flow
studies after 20 years: a role in stream management and restoration, Regulated Rivers:
Research and Management 17 (2001), pp. 527–542. Abstract-GEOBASE | Order
Document | Full Text via CrossRef
Gower et al., 1994 A.M. Gower, G. Myers, M. Kent and M.E. Foulkes, Relationships
between macroinvertebrate communities and environmental variables in metalcontaminated streams in south-west England, Freshwater Biology 32 (1994), pp. 199–
221. Abstract-GEOBASE | Order Document | Full Text via CrossRef
Hall et al., 1986 W.S. Hall, K.L. Dickson, F.Y. Saleh and J.H. Rodgers, Effects of
suspended solids on the bioavailability of chlordane to Daphnia magna, Archives of
Environmental Contamination and Toxicology 15 (1986), pp. 529–534. AbstractEMBASE | Order Document | Full Text via CrossRef
Herbert, 2003 Herbert, S., 2003. The impact of lawn care practices on suburban streams
in metropolitan Atlanta, Georgia. Master's thesis. University of Georgia, Athens, GA,
USA.
IJC, 1977 International Joint Council (IJC), 1977. New and revised great lakes water
quality objectives. IJC, Canada and USA.
Kadlec and Benson, 1995 M.C. Kadlec and W.H. Benson, Relationship of aquatic natural
organic material characteristics to the toxicity of selected insecticides, Ecotoxicology and
Environmental Safety 31 (1995), pp. 84–97. Abstract | PDF (834 K)
Larson et al., 1999 Larson, S.J., Gilliom, R.J., Capel, P.D., 1999. Pesticides in streams of
the United States – initial results from the National Water Quality Assessment Program.
US Geological Survey Water Resources Investigation Report 98-4222, Sacramento, CA,
USA.
Lenat, 1993 D.R. Lenat, A biotic index for the southeastern United States: derivation and
list of tolerance values, with criteria for assigning water-quality ratings, Journal of the
North American Benthological Society 12 (1993), pp. 279–290.
Lloyd et al., 1987 D.S. Lloyd, J.P. Koenings and J.D. LaPerriere, Effects of turbidity in
fresh waters of Alaska, North American Journal of Fisheries Management 7 (1987), pp.
18–33. Full Text via CrossRef
Medeiros et al., 1983 C. Medeiros, R. LeBlanc and R.A. Coler, An in situ assessment of
the acute toxicity of urban runoff to benthic macroinvertebrates, Environmental
Toxicology and Chemistry 2 (1983), pp. 119–126. Abstract-GEOBASE | Order
Document
Merrit and Cummins, 1996 R.W. Merritt and K.W. Cummins, Introduction to the Aquatic
Insects of North America, Kendall/Hunt, Dubuque, IA, USA (1996).
Minshall, 1981 G.W. Minshall, Structure and temporal variations of the benthic
macroinvertebrate community inhabiting Mink Creek, Idaho, USA., a 3rd order Rocky
Mountain stream, Journal of Freshwater Ecology 1 (1981), pp. 13–26.
Munn and Gilliom, 2001 Munn, M.D., Gilliom, R.J., 2001. Pesticide toxicity index for
freshwater aquatic organisms. U.S. Geological Survey, Water-Resources Investigation
Report 01-4077, National Water-Quality Assessment Program, Sacramento, CA, USA.
Richardson and Kiffney, 2000 J.S. Richardson and P.M. Kiffney, Responses of a
macroinvertebrate community from a pristine, southern British Columbia, Canada, stream
to metals in experimental mesocosms, Environmental Toxicology and Chemistry 19
(2000), pp. 736–743. Abstract-EMBASE | Abstract-GEOBASE | Abstract-Elsevier
BIOBASE | Order Document | Full Text via CrossRef
Rosenberg and Resh, 1996 D.M. Rosenberg and V.H. Resh, Use of aquatic insects in
biomonitoring. In: R.W. Merritt and K.W. Cummins, Editors, Introduction to the Aquatic
Insects of North America, Kendall/Hunt, Dubuque, IA, USA (1996), pp. 87–97.
Roy et al., 2003a A.H. Roy, A.D. Rosemond, M.J. Paul, D.S. Leigh and J.B. Wallace,
Stream macroinvertebrate response to catchment urbanisation (Georgia, USA),
Freshwater Biology 48 (2003), pp. 329–346. Abstract-Elsevier BIOBASE | AbstractGEOBASE | Order Document | Full Text via CrossRef
Roy et al., 2003b A.H. Roy, A.D. Rosemond, D.S. Leigh, M.J. Paul and J.B. Wallace,
Habitat-specific responses of stream insects to land cover disturbance: biological
consequences and monitoring implications, Journal of the North American Benthological
Society 22 (2003), pp. 292–307. Abstract-Elsevier BIOBASE | Abstract-GEOBASE |
Order Document
Ruse et al., 2000 L.P. Ruse, S.J. Herrmann and J.E. Sublette, Chironomidae (Diptera)
species distribution related to environmental characteristics of the metal-polluted
Arkansas River, Colorado, Western North American Naturalist 60 (2000), pp. 34–56.
Abstract-Elsevier BIOBASE | Order Document
Sokal and Rohlf, 1995 R.R. Sokal and F.J. Rohlf, Biometry (third ed.), W.H. Freeman
and Company, New York, USA (1995).
Statzner, 1981 B. Statzner, A method to estimate the population size of benthic
macroinvertebrates in streams, Oecologica 51 (1981), pp. 157–161. Full Text via
CrossRef
Stuijfzand et al., 2000 S.C. Stuijfzand, L. Poort, G.D. Greve, H.G. van der Geest and
M.H.S. Kraak, Variables determining the impact of diazinon on aquatic insects: taxon,
developmental stage, and exposure time, Environmental Toxicology and Chemistry 19
(2000), pp. 582–587. Abstract-EMBASE | Abstract-GEOBASE | Abstract-Elsevier
BIOBASE | Order Document | Full Text via CrossRef
Suedel et al., 1996 B.C. Suedel, E. Deaver and J.H. Rodgers Jr., Experimental factors that
may affect toxicity of aqueous and sediment-bound copper to freshwater organisms,
Archives of Environmental Contamination and Toxicology 30 (1996), pp. 40–46.
Abstract-EMBASE | Order Document | Full Text via CrossRef
US EPA, 1991 United States Environmental Protection Agency (US EPA), 1991. Water
quality criteria summary. Wall Poster, US EPA, Office of Water, Office of Science and
Technology, Health and Ecological Effects Division, Washington, DC, USA.
US EPA, 2002 United States Environmental Protection Agency (US EPA), 2002.
National recommended water quality criteria: 2002. EPA-822-R-02-047. US EPA, Office
of Water, Office of Science and Technology (4304T), Washington, DC, USA.
USGS, 1999 United States Geological Survey (USGS), The quality of our nation's waters
– nutrients and pesticides, U.S. Geological Survey Circular 1225 (1999) (Reston, VA,
USA).
Wallace et al., 1996 J.B. Wallace, J.W. Grubaugh and M.R. Whiles, Biotic indices and
stream ecosystem processes: results from an experimental study, Ecological Applications
6 (1996), pp. 140–151. Full Text via CrossRef
Winget and Mangum, 1979 R.N. Winget and F.A. Mangum, Biotic Condition Index:
Integrated Biological, Physical and Chemical Stream Parameters for Management,
Intermountain Region, U.S. Department of Agriculture, Forest Service, Ogden, UT, USA
(1979).
Wolman, 1954 M.G. Wolman, A method of sampling coarse river-bed material,
Transactions, American Geophysical Union 35 (1954), pp. 951–956.
Zar, 1999 J.H. Zar, Multiple comparisons, Biostatistical Analysis (fourth ed.), PrenticeHall, Upper Saddle River, NJ, USA (1999) pp. 208–230.
Corresponding author. Tel.: +1 706 542 1184; fax: +1 706 542 2279.
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