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    Map of Tanyard Creek showing significant landmarks; locations of sampling sites are marked with the sample site number.

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    Prevalence of mosquito larvae and pupae (by dipping) and the cumulative water volume released from the Tanyard Creek CSO facility during the 5 days prior to sampling. Model: y = 44.6 × exp(−0.0002x).

  • View in gallery

    Association between prevalence of positive mosquito samples (by dipping) and the average rate of water flow from the Tanyard Creek CSO facility during events 1–5 days prior to sampling. Model: y =45.95 × exp(−0.1392x).

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    Prevalence of positive dips for mosquito larvae after a flooding event exceeding 15 kgal/min in Tanyard Creek.

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    Mosquito species identified from pupae collected in Tanyard Creek during 2005.

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    Geometric mean numbers of mosquito immatures samples by stage and study site in Tanyard Creek from June through November 2005.

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Combined Sewage Overflows (CSO) Are Major Urban Breeding Sites for Culex quinquefasciatus in Atlanta, Georgia

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  • 1 Division of Parasitic Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia

A longitudinal study of mosquito ecology in Tanyard Creek, an urban stream in Atlanta, GA, that receives combined storm and waste water effluent from the Atlanta combined sewage overflow system, was undertaken in 2006. Culex quinquefasciatus was the dominant species found, but Culex restuans was also abundant during the spring with limited numbers of Culex nigripalpis and Anopheles punctipennis also collected. Significant differences in mosquito densities were found with greater densities associated with side pools of water and stagnant water. Mosquito numbers are regulated largely by flooding of the stream by effluent discharges exceeding 15 kgal/min. These floods are associated with significant immediate reductions, but not complete elimination, of mosquitoes from Tanyard Creek. Mosquito numbers rebound within 5–10 days after such floods and rapidly reach high densities.

INTRODUCTION

Prior to 1999, West Nile Virus (WNV), a mosquitoborne flavivirus, was found in Africa, Europe, and the Middle East.1,2 In the summer of 1999, WNV was detected in an outbreak in New York City.3 In the ensuing years, WNV spread throughout the United States, Canada, and the Caribbean, resulting in > 16,000 human infections and 686 deaths.1,4 In 2005, there were 2,949 WNV cases in the United States, including 1,288 cases with neuroinvasive disease and 116 deaths (E. Farnon, 2006 WNV Conference, unpublished data).

The virus is maintained in a mosquito–bird transmission cycle with humans, horses, and other mammals being dead-end hosts. Enzootic maintenance of WNV depends on juxtaposition of susceptible bird and vector populations and presence of the virus. Transmission to humans requires a bridge vector for the virus between the bird and human populations. Although > 60 mosquito species have tested positive for the WNV, members of the Culex pipiens complex (Cx. pipiens and Culex quinquefasciatus) and Culex tarsalis are dominant species in the enzootic maintenance and amplification of this virus in the United States.1,5 These species may also serve as possible bridge vectors to humans. Field studies in the southeastern United States incriminated Cx. quinquefasciatus as the principal WNV vector in Florida,6,7 Georgia, and Louisiana.79

In 2005, 66 mosquito pools from Georgia were positive by PCR for WNV; 63 of the WNV-positive pools contained Cx. quinquefasciatus. The remaining positive samples were from 2 Culex restuans and 1 Culex nigrapalpus pool (R. Kelly, Georgia State Health Department, unpublished data). Cx. quinquefasciatus is primarily ornithophilic,5 but it is a possible bridge vector when feeding on mammals.10,11 Culex species are also vectors of St. Louis encephalitis virus and can be major nuisance species in urban areas. Cx. quinquefasciatus breeds in many different water sources, attaining high larval densities in water with high organic content, such as sewage treatment ponds, drains,12,13 and pit latrines.14

Many urban areas in the United States, particularly in the northeastern and central states, have combined waste and storm water systems, known as combined sewage overflows (CSOs), for treating and disposing of water. In this system, during normal operating conditions, minimally treated waste-water and storm water are mixed and then piped to a waste water treatment facility. However, during times of heavy precipitation when water volumes exceed the capacity of the water treatment facilities, the combined waste and storm water bypasses the treatment facility to be discharged directly into streams or lakes after only minimal chlorine treatment and sieving of large physical contaminants at the CSO facility. These overflows or “events” result in the release of untreated human and industrial waste, toxic materials, and debris. Regulators differ from CSO facilities in that the mixed storm and waste water received by a regulator is directed to a water treatment plant during dry weather but is diverted to a CSO facility during times of heavy precipitation without providing either chlorine treatment or sieving.

More than 772 communities are affected by CSOs in the United States (http://cfpub.epa.gov/npdes/home.cfm?program_id=5). Effluents from these CSOs create potential breeding sites for Culex spp. If streams receiving CSO effluent are used by Culex spp. for oviposition, the potential for the transmission of Arboviruses including WNV and St. Louis encephalitis virus transmission in urban areas could be significantly enhanced. The City of Atlanta has 7 CSOs and 2 regulators. Streams receiving effluent from CSO facilities and regulators will be referred to henceforth as “CSO streams.” These CSO streams in Atlanta are centrally located in close proximity to residential, commercial, and recreational areas.

The overall goal of this study was to define the role of CSO streams for WNV vector mosquito production in Atlanta, GA. Specific objectives for this study of CSO streams were 1) to identify the mosquito species utilizing the streams, 2) to determine the environmental factors associated with increased mosquito densities, and 3) to understand the primary factors that regulate mosquito populations in these streams.

MATERIALS AND METHODS

Field sites.

The study took place in the 3.4-km section of Tanyard Creek, ≈0.5 km downstream from the Tanyard Creek CSO facility in Atlanta, GA, to where it joins Peach-tree Creek in the Bobby Jones Golf Course (Figure 1). Although Tanyard Creek above the study section is paved with concrete, the section of Tanyard Creek selected for study appears as a natural urban stream/creek habitat running through densely populated residential areas of Atlanta with public access at multiple sites including Ardmore Park, Collier Road, Bitsy Grant Tennis Center, and Bobby Jones Golf Course. Tanyard Creek is ≈10–15 m in width with a non-flood depth ranging from 1 to 2 m.

Tanyard Creek was mapped with a Garmin 60CS GPS unit. Eight sites within the Tanyard Creek study area were selected as representative habitats for detailed larval and pupal surveys. Weekly mosquito larval surveys of Tanyard Creek were conducted from June 29, 2005, through October 27, 2005, with less frequent sampling until December 12, 2005. Mosquito populations were sampled by dipping. For a control, Rock Creek in the H. Taylor and D. Johnston Nature Preserve (located ≈3 miles east of Tanyard Creek) was sampled in a similar manner to Tanyard Creek. Rock Creek is a natural urban stream in the City of Atlanta that receives runoff from city streets but not wastewater effluent.

Surveys in Tanyard Creek consisted of 25 dips at each of the 8 sites (total of 200 dips/survey). Numbers of egg rafts, early instars (first and seconds), later instars (thirds and fourths), and pupae were counted for each dip and recorded. Egg rafts were transferred with a wooden applicator to 50-mL centrifuge tubes for transport to the laboratory with water samples from the CSO stream. All captured pupae were transferred to 50-mL conical centrifuge tubes for transportation to the laboratory. Adults were allowed to emerge prior to identification using the taxonomic keys of Darsie and Morris.15

The habitat of each dip was defined and categorized. Bottom substrates were categorized as sandy, rocky/pebbly, or rock slab. Water flow rate was described as stagnant, slow or fast. Stagnant water was defined as having no visible water movement. Slowly moving water had barely perceptible surface movement, and fast water was defined as having obvious surface movement with agitation. Data on sunlight was dichotomized as either sunny or shady. Habitat locations were defined by pool size/type as being 1) a pool (i.e., being completely separated from the main creek), 2) the side or bank of the creek, or 3) located in the middle of the creek. Water-quality information was recorded as clear, cloudy/murky, rusty in color, or with visible surface oil.

Other species (insects, fish, etc.) encountered during the surveys were noted. Information on events was provided by the CSO facility manager and included duration, volume, and date of effluent discharge into Tanyard Creek.

Statistical analysis.

Geometric means were calculated by exponentiating the log mean of the counts then subtracting 1 (1 was initially added to each count to derive log values on zero values). Poisson regression was used to compare mean counts by site and environmental characteristic. Regressions were run using SAS Proc Genmod (SAS, Inc., Cary, NC) implementing the generalized estimating equations (GEE) procedure to take into consideration the longitudinal aspect of the study and to adjust for the correlation among multiple observations from the same site. When making multiple comparisons, the α level of each individual test was adjusted downward using the Bonferroni method to adjust for the increased risk of at least one spuriously significant result and to ensure that the per-experiment risk remains at 0.05. A 2-parameter exponential model was used to show the association between percent positive collections and average rate and/or volume of water released from the CSO. Statistical analyses were performed using SAS version 9.1 and/or SigmaPlot 2000 (SPSS, Chicago, IL). Statistical significance was set at α = 0.05.

RESULTS

In 2005, there were 567 discharges of effluent from the 7 CSO facilities and 2 regulators into urban streams in Atlanta (J. Shimmin, personal communication). During the 166 days that mosquito populations were monitored in Tanyard Creek, effluent was discharged from the CSO facility on 64 days. These events ranged in discharge volume from 104 kilogallons during 36 minutes to 173,366 kilogallons over a 28-hr period. An inverse relationship was found between the volume of water released in the previous 1–5 days and the prevalence of dips positive for any mosquito stage (Figure 2). When > 10,000 kilogallons of effluent were discharged from the CSO facility during the 5 days prior to sampling, very few larval mosquitoes were captured during the surveys of Tanyard Creek. Alternatively stated, flow rates > 15 kilogallons/minute eliminated almost all larval mosquitoes in Tanyard Creek (Figure 3). Significant increases in the proportion of dips positive for mosquito stages were found within 5–10 days of an event (Figure 4).

Cx. quinquefasciatus and Cx. restuans were the dominant species identified from pupae collected in Tanyard Creek; 58% and 42% of the larval mosquito populations in Tanyard Creek during June were Cx. quinquefasciatus and Cx. restuans, respectively (Figure 5). The proportion of immatures that were Cx. quinquefasciatus increased steadily from June through October when only Cx. quinquefasciatus pupae were found. However, in November, 65% of adults identified from pupae were Cx. restuans. Mosquito immatures were not found during the December 12, 2005, survey. In addition, a small number of Anopheles punctipennis (N = 1) and Cx. nigripalpus (n = 4) were identified from pupae found in Tanyard Creek.

Significant differences in the geometric mean (gm) number of all mosquito immature stages per dip were found among the 8 sites (Figure 6). Densities of all mosquito immature stages ranged from 0 to > 500/dip. Site 3 had significantly lower densities of all immature mosquito stages than sites 5 and 8 (P ≤ 0.0010). Egg rafts were found at significantly higher densities at site 2 (gm = 0.09; range: 0–18/dip) than at any of the other 7 survey sites. Site 1 had significantly lower densities (gm = 0.14; range: 0–50/dip) of early stage larvae than sites 2, 5, 7, and 8 (P < 0.0001) while site 3 had significantly less late-stage larvae per dip (gm = 0.17; range: 0–50) than was found at sites 5 and 8 (P < 0.0001). Pupae were found at significantly higher densities at site 8 (gm = 0.11; range: 0–101) than at sites 2, 6, and 7 (P < 0.0003).

The densities of the immature mosquitoes varied significantly (P < 0.017) among sampling locations in Tanyard Creek (namely, side pools, banks of the main channel, and middle of the stream; Table 1). For all immature stages except pupa, density was significantly higher in side pools, lower in stream banks, and lowest in midstream. Although pupae were numerically denser in side pools compared with midstream, the difference was borderline significant. All immature life stages preferred shady to sunny locations, but this difference was only statistically significant for early instar larvae (P < 0.025). In contrast, immature mosquitos were rare in the non-CSO control stream of Rock Creek: 200 dips from Rock Creek yielded a total of only 2 early instar larvae (one Anopheles species and one unidentifiable culicine).

Water movement played a major role on densities of immature mosquitoes with significantly (P < 0.0100) greater numbers of all stages (except egg rafts) found in stagnant compared with fast-moving water (Table 1). Significantly more late larval instars and pupa were found in slow- versus fast-moving water as well (P < 0.0042). A statistically significant difference between stagnant water and slow water in the geometric mean numbers of egg rafts per dip (gm = 0.036 and 0.006, respectively) was also present (P < 0.0167).

Water quality was an important factor in densities of immature mosquitoes. The highest densities for all stages were found in oily and/or rusty water, the lowest densities in clear water and/or cloudy/murky water. Compared with clear water counts, statistically higher densities were seen for egg rafts in oily, rusty, or cloudy/murky water (P < 0.0001); for pupa in cloudy/murky waters (P < 0.0001); for early instars in rusty and cloudy/murky waters (P < 0.0001); and for late instars in rusty water (P < 0.0001). (Table 1).

Bottom substrates played an important, though lesser, role in immature mosquito populations. Egg rafts and early instars showed no preference for sandy, rock slab, or pebbly substrates, whereas late instar density was significantly higher (P < 0.006) on sandy bottom substrates and rock slabs than rocky/pebbly bottoms. Sandy substrates were also associated with higher-density pupae (P = 0.003).

Other invertebrates were collected during sampling for mosquitoes. Midges (family: Chironomidae) were the most frequently captured nonmosquito invertebrate. Dragonfly nymphs and beetles were rarely seen; fish were only seen near the mouth of Tanyard Creek where it empties into Peachtree Creek.

DISCUSSION

In 1999, the City of Atlanta was found in violation of both the federal Clean Water Act and the Georgia Water Quality Control Act resulting from the discharge of effluent from CSO facilities into urban streams that empty into the Chattahoochee River. The settlement with the EPA required the City of Atlanta to 1) pay a $3.2 million fine (the largest Clean Water Act penalty ever assessed against a municipality [http://yosemite.epa.gov/opa/admpress.nsf/016bcfb1deb9fecd85256aca005d74df/1d9bf67474410410852567bd0073d60c!OpenDocument]), 2) eliminate all discharges, and 3) implement detailed programs for CSO management within 14 years (minutes from City Council). The second term of the settlement requires (at a cost of $3.9 billion) the construction of an underground reservoir system to hold excess effluent during times of heavy precipitation until water treatment plants can process the material. The settlement addressed the environmental impacts of the CSO system on the streams and rivers in Atlanta but did not consider the impacts of either the present or the future CSO systems on mosquito populations.

This study documents that urban streams and creeks in Atlanta that receive effluent from regulators and CSO facilities can be major breeding sites for Cx. quinquefasciatus and Cx. restuans mosquitoes. Cx. quinquefasciatus was the dominant species in Tanyard Creek during the summer and early fall and was the mosquito species from which 95% of WNV positive-mosquito pools were detected in Georgia during 2005. Cx. restuans was also abundant in early summer, and populations of this mosquito resurged in late fall. WNV was also detected in this mosquito in Georgia in 2005.

All sections of Tanyard Creek were not equally productive for the immature stages of Culex mosquitoes: mosquito larvae and pupae achieved highest densities in isolated pools found along the banks of Tanyard Creek. Highest mosquito densities were also associated with stagnant and slow-moving water with sandy bottom substrates. Clear water contained the lowest densities of immature mosquitoes, and oily and rusty water was associated with significantly higher mosquito densities.

The combined waste and storm water in CSO streams such as Tanyard Creek provides an optimal environment for the larvae of Cx. quinquefasciatus and Cx. restuans. The organically rich water provides an ample food supply while at the same time creating an unfavorable environment for mosquito predators due to the diminished oxygen concentrations; invertebrate predators (e.g., dragonfly nymphs) were rarely noted in the CSO stream, whereas fish were seen only where Tanyard Creek empties into Peachtree Creek.

Ironically, immature mosquito populations in CSO creeks appear to be predominantly regulated by the same water-flow patterns that result in the release of pollutants that eventually flow into the Chattahoochee River. Flooding of the CSO basin with waste and storm water also flushes most mosquito larvae and pupae downstream. Although flooding significantly reduces the mosquito populations in the CSO creek, larvae and pupae are not eliminated entirely. The weekly time frame for sampling in this study did not permit precise estimation of the time needed for mosquito populations to rebound from flooding events. However, significant increases in the densities of lateinstar larvae and pupae were seen 5–10 days after flooding.

CSOs have the potential to produce large numbers of Cx. quinquefasciatus, depending on the water-flow patterns. Infrequent flooding could increase the risk of urban transmission of WNV within the flight range of Cx. quinquefasciatus by allowing rapid buildups in the larvae of vectors that breed in the CSO streams. The 9 CSOs and regulators in the City of Atlanta presently experience hundreds of flooding events per year. If the City of Atlanta has a drought, conditions would be ideal for mosquito production in the CSO streams. It is uncertain what the impact of the remediation system to prevent pollution of the Chattahoochee River will be. The new CSO system, designed to minimize pollution of the Chattahoochee River, is scheduled for completion in 2007. It is estimated that combined storm and waste water events would occur < 10 times per year after completion of the system under construction. This amount of flooding could potentially maintain an ideal environment in CSO streams for Cx. quinquefasciatus, the primary WNV vector in Georgia: infrequent flooding could maintain a high organic content in the streams with minimal flushing of mosquitoes downstream.

Further monitoring of mosquito populations in CSO streams in Atlanta is needed to determine if the CSO remediation system will facilitate the growth of mosquito populations. As the new system is scheduled to be operational in 2007, there is an urgent need to evaluate interventions to control both larval populations in streams and emergency adult control strategies.

Table 1

Density of mosquito stages per dip in relation to CSO stream characteristics

Mosquito stage
Egg rafts1st and 2nd instars3rd and 4th instarsPupae
CharacteristicGeometric mean (95% C.L.) No. of mosquitoes No. of dipsP valueGeometric mean (95% C.L.) No. of mosquitoes No. of dipsP valueGeometric mean (95% C.L.) No. of mosquitoes No. of dipsP valueGeometric mean (95% C.L.) No. of mosquitoes No. of dipsP value
* Significant at α = 0.05.
** Significant at Bonferroni adjusted α = 0.0167. ^ Significant at Bonferroni adjusted α = 0.0083.
Water flow rate
    Stagnant0.036 (0.020, 0.051)0.1290.408 (0.323, 0.499)0.0004**0.478 (0.391, 0.569)< 0.0001**0.078 (0.052, 0.105)0.010**
7122272050271
833833824823
    Slow.0059 (0.002, 0.103)0.1110.213 (0.169, 0.259)0.1310.285 (0.233, 0.339)< 0.0001**0.053 (0.037, 0.069)0.004**
1111381716138
1120112111121110
    Fast0.010 (0, 0.030)Referent0.062 (0, 0.144)Referent0.070 (0, 0.147)Referent0.005 (0, 0.015)Referent
382691
140140140140
Relative sunlight
    Shady0.026 (0.015, 0.038)0.1440.336 (0.274, 0.402)< 0.0001*0.412 (0.347, 0.480)0.0680.065 (0.045, 0.086)0.328
8726452382165
1166116711491144
    Sunny0.001 (0.000, 0.020)Referent0.2313 (0.169, 0.297)Referent0.277 (0.209, 0.349)Referent0.051 (0.032, 0.070)Referent
21950126574
690690688688
Location
    Side pool0.062 (0.031, 0.094)< 0.0001**0.624 (0.466, 0.798)< 0.0001**0.617 (0.468, 0.780)< 0.0001**0.097 (0.056, 0.139)< 0.038
7918811815198
430430429427
    Stream bank0.019 (0.012, 0.026)0.011**0.324 (0.276, 0.374)< 0.0001**0.372 (0.322, 0.423)< 0.0001**0.061 (0.047, 0.076)0.626
7735963484293
1825182618171814
    Stream middle0.010 (0.002, 0.018)Referent0.143 (0.095, 0.193)Referent0.190 (0.139, 0.244)Referent0.042 (0.023, 0.063)Referent
1462562392
692692683683
Substrate
    Rock slab0.014 (0.004, 0.024)0.64910.327 (0.246, 0.413)0.03860.429 (0.331, 0.536)0.0059**0.079 (0.049, 0.110)0.0538
1912552082187
659659652650
    Sandy0.019 (0.012, 0.026)0.65920.297 (0.244, 0.352)0.03550.391 (0.331, 0.454)0.0024**0.080 0.059, 0.102)0.0031**
4222452879460
1326132713171316
    Rocky/pebbly0.018 (0.010, 0.025)Referent0.207 (0.169, 0.247)Referent0.253 (0.213, 0.296)Referent0.047 (0.033, 0.060)Referent
5714861492186
1474147514621460
Water quality
    Rusty0.111 (0.027, 0.201)< 0.0001^1.009 (0.547, 1.625)< 0.0001^1.031 (0.294, 0.395)< 0.0001^0.064 (0.048, 0.081)0.2292
2893658731
98989898
    Oily0.079 (0.041, 0.120)< 0.0001^0.420 (0.277, 0.579)0.09150.448 (0.300, 0.614)0.05800.076 (0.035, 0.119)0.1539
60104499375
303303303303
    Cloudy/murky0.058 (0.034, 0.083)< 0.0001^0.255 (0.164, 0.352)< 0.0001^0.338 (0.238, 0.447)0.02820.103 (0.056, 0.151)< 0.0001^
5914801270394
486486486486
    Clear0.005 (0.001, 0.009)Referent0.289 (0.239, 0.339)Referent0.344 (0.294, 0.395)Referent0.064 (0.049, 0.081)Referent
1318671797212
1386138713691366
Figure 1.
Figure 1.

Map of Tanyard Creek showing significant landmarks; locations of sampling sites are marked with the sample site number.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 77, 3; 10.4269/ajtmh.2007.77.478

Figure 2.
Figure 2.

Prevalence of mosquito larvae and pupae (by dipping) and the cumulative water volume released from the Tanyard Creek CSO facility during the 5 days prior to sampling. Model: y = 44.6 × exp(−0.0002x).

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 77, 3; 10.4269/ajtmh.2007.77.478

Figure 3.
Figure 3.

Association between prevalence of positive mosquito samples (by dipping) and the average rate of water flow from the Tanyard Creek CSO facility during events 1–5 days prior to sampling. Model: y =45.95 × exp(−0.1392x).

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 77, 3; 10.4269/ajtmh.2007.77.478

Figure 4.
Figure 4.

Prevalence of positive dips for mosquito larvae after a flooding event exceeding 15 kgal/min in Tanyard Creek.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 77, 3; 10.4269/ajtmh.2007.77.478

Figure 5.
Figure 5.

Mosquito species identified from pupae collected in Tanyard Creek during 2005.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 77, 3; 10.4269/ajtmh.2007.77.478

Figure 6.
Figure 6.

Geometric mean numbers of mosquito immatures samples by stage and study site in Tanyard Creek from June through November 2005.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 77, 3; 10.4269/ajtmh.2007.77.478

*

Address correspondence to Thomas R. Burkot, Division of Parasitic Diseases, Centers for Disease Control and Prevention, 4770 Buford Hwy., MS F-42, Atlanta, GA 30341. E-mail: Tburkot@cdc.gov

Authors’ addresses: Lisa M. Calhoun, Melissa Fox, LeeAnn Jones, Karina Gunarto, Raymond King, Jacquelin Roberts, and Tom Burkot, Division of Parasitic Diseases, Centers for Disease Control and Prevention, 4770 Buford Hwy., MS F-42, Atlanta, GA 30341, Telephone: +1 (770) 448-3607, Fax: +1 (770) 488-4258, E-mail: Tburkot@cdc.gov.

Acknowledgments: The authors thank Jerry Kerce of Fulton County Department of Health and Wellness to alerting us to the potential of CSO streams for mosquito breeding and for his support and enthusiasm for this project. Special thanks to John Shimmin, CSO facilities manager for City of Atlanta, for generously sharing both his knowledge of CSOs and information on CSO events in Atlanta; to Dr. Robert A. Wirtz, CDC, for his critical review of the manuscript; to Jodi Vander Eng for producing the map of Tanyard Creek CSO (Figure 1); and to Dr. Ellen Dotson, the mentor of Lisa Calhoun. In addition, we acknowledge the assistance of Stephen Burkot in sampling Rock Creek.

Financial support: This research was supported, in part, by the Emerging Infectious Diseases (EID) Fellowship Program administered by the Association of Public Health Laboratories (APHL) and funded by the Centers for Disease Control and Prevention (CDC).

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Author Notes

Reprint requests: Tom Burkot, Division of Parasitic Diseases, Centers for Disease Control and Prevention, 4770 Buford Hwy., MS F-42, Atlanta, GA 30341, E-mail: Tburkot@cdc.gov.
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